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Full text of "Malacologia"

HARVARD UNIVERSITY 

Library of the 

Museum of 

Comparative Zoology 



VOL. 36, NO. 1-2 MALACOLOGIA 1995 

CONTENTS 

MARÍA VILIJVRROEL Y JOSÉ STUARDO 

Morfología del Estomago y Partes Blandas en Mytella strigata (Hanley, 1843) 
(Bivalvia: Mytilidae) 1 

JOST BORCHERDING 

Laboratory Experiments on the Influence of Food Availability, Temperature and 
Photoperiod on Gonad Development in the Freshwater Mussel Dreissena 
Polymorpha 15 

R. ARAUJO, J. M. REMÓN, D. MORENO & M. A. RAMOS 

Relaxing Techniques for Freshwater Molluscs: Trials for Evaluation of Different 
Methods 29 

KENNETH С EMBERTON 

Land-Snail Community Morphologies of the Highest-Diversity Sites of Mada- 
gascar, North America, and New Zealand, with Recommended Alternatives to 
Height-Diameter Plots 43 

KENNETH С EMBERTON 

Distributional Differences Among Acavid Land Snails Around Antalaha, Mada- 
gascar: Inferred Causes and Dangers of Extinction 67 

KATHERINE COSTIL & JACQUES DAGUZAN 

Effect of Temperature on Reproduction in Planorbarius comeus (L) and Plan- 

orbis planorbis (L.) Throughout the Life Span 79 

L M. COOK & J. BRIDLE 

Colour Polymorphism in the Mangrove Snail Littoraria intermedia in Sinai 91 

MICHAEL G. GARDNER, PETER B. MATHER, IAN WILLIAMSON & JANE M. HUGHES 

The Relationship Between Shell-Pattern Frequency and Microhabitat Variation 

in the Intertidal Prosobranch, Clithon oualaniensis (Lesson) 97 

MIGUEL IBÁÑEZ, ELENA PONTE-LIRA & MARÍA R. ALONSO 

El Género Canañella Hesse, 1918, y su Posición en la Familia Hygromiidae 
(Gastropoda, Pulmonata, Helicoidea) Ill 

N. ELEUTHERIADIS & M. LAZARIDOU-DIMITRIADOU 

Age-Related Differential Catabolism in the Snail Bithynia graeca (Westerlund, 

1879) and its Significance in the Bioenergetics of Sexual Dimorphism 139 

HEINZ BRENDELBERGER 

Dietary Preference of Three Freshwater Gastropods for Eight Natural Foods of 
Different Energetic Content 1 47 

ROBERT H. COWIE, GORDON M. NISHIDA, YVES BASSET & SAMUEL M. GON, III 

Patterns of Land Snail Distribution in a Montane Habitat on the Island of 
Hawaii 1 55 

AU\N E. STIVEN 

Genetic Heterozygosity and Growth Rate in the Southern Appalachian Land 

Snail Mesodon normalis (Pilsbry 1900): The Effects of Laboratory Stress 171 

DAVID R. LAWRENCE 

Diagnosis of the Genus Crassostrea (Bivalvia, Ostreidae) 1 85 

KENNETH С EMBERTON & SIMON TILLtER 

Clarification and Evaluation of Tillier's (1989) Stylommatophoran Mono- 
graph 203 



VOL. 37, NO. 1 1995 



MALACÖLOGIA 



International Journal of Malacology 
Revista Internacional de Malacologia 
Journal International de Malacologie 
Международный Журнал Малакологии 
Internationale Malakologische Zeitschrift 



MALACOLOGIA 

Editor-in-Chief: 
GEORGE M. DAVIS 

Editorial and Subscription Offices: 

Department of Malacology 

The Academy of Natural Sciences of Philadelphia 

1900 Benjamin Franklin Parkway 

Philadelphia, Pennsylvania 19103-1195, U.S.A. 



Co-Editors: 



EUGENE COAN 

California Academy of Sciences 

San Francisco, CA 



CAROL JONES 
Denver, CO 



Assistant Managing Editor: 

CARYL HESTERMAN 

Associate Editors: 



JOHN B. BURCH 
University of Michigan 
Ann Arbor 



ANNE GISMANN 

Maadi 

Egypt 



MALACOLOGIA is published by the INSTITUTE OF MALACOLOGY, the Sponsor Members of 
which (also serving as editors) are: 



RÜDIGER BIELER 
Field Museum,. Chicago 

JOHN BURCH 

MELBOURNE R. CARRIKER, 

President Elect 

University of Delaware, Lewes 

GEORGE M. DAVIS 
Secretary and Treasurer 

CAROLE S. HICKMAN, President 
University of California, Berkeley 



AU\N KOHN 

University of Washington, Seattle 

JAMES NYBAKKEN 

Moss Landing Marine Laboratory 

California 

CLYDE F. E. ROPER 
Smithsonian Institution 
Washington, D.C. 

SHI-KUEI WU 

University of Colorado Museum, Boulder 



' Participating Members 

EDMUND GITTENBERGER JACKIE L VAN GOETHEM 

Secretary, UNITAS MALACOLOGICA Treasurer, UNITAS MALACOLOGICA 

Rijksmuseum van Natuurlijke Koninklijk Belgisch Instituut 

Historie voor Natuurwetenschappen 

Leiden, Netherlands Brüssel, Belgium 



J. FRANCIS ALLEN, Emérita 
Environmental Protection Agency 
Washington, D.C. 

KENNETH J. BOSS 

Museum of Comparative Zoology 

Cambridge, Massachusetts 



Emeritus Members 

ROBERT ROBERTSON 

The Academy of Natural Sciences 

Philadelphia, Pennsylvania 

W. D. RUSSELL-HUNTER 
Easton, Maryland 



Copyright ç 1995 by the Institute of Malacology 



1995 
EDITORIAL BOARD 



J. A. ALLEN 

Marine Biological Station 

Millport, United Kingdom 

E. E. BINDER 

Muséum d'Histoire Naturelle 

Genève, Switzerland 

A. J. CAIN 

University of Liverpool 
United Kingdom 

P. CALOW 

University of Sheffield 
United Kingdom 

J. G. CARTER 

University of North Carolina 

Chapel Hill, U.S.A. 

R. COWIE 
Bishop Museum 
Honolulu, HI., U.S.A. 

A. H. CLARKE, Jr. 
Portland, Texas, U.S.A. 

B. С CLARKE 
University of Nottingham 
United Kingdom 

R. DILLON 

College of Charleston 

SC, U.S.A. 

C. J. DUNCAN 
University of Liverpool 
United Kingdom 

D. J. EERNISSE 
California State University 
Fullerton, U.S.A. 

E. GITTENBERGER 

Rijksmuseum van Natuurlijke Historie 
Leiden, Netherlands 

F. GIUSTI 

Université di Siena, Italy 

A. N. GOLIKOV 
Zoological Institute 
St. Petersburg, Russia 



S. J. GOULD 
Harvard University 
Cambridge, Mass., U.S.A. 

A. V. GROSSU 
Universitatea Bucuresti 
Romania 

T. HABE 
Tokai University 
Shimizu, Japan 

R. HANLON 

Marine Biomedical Institute 

Galveston, Texas, U.S.A. 

J. A. HENDRICKSON, Jr. 
Academy of Natural Sciences 
Philadelphia, PA, U.S.A. 

D. M. HILLIS 
University of Texas 
Austin, U.S.A. 

K. E. HOAGLAND 

Association of Systematics Collections 

Washington, DC, U.S.A. 

B. HUBENDICK 
Naturhistohska Museet 
Göteborg, Sv^^eden 

S. HUNT 
Lancashire 
United Kingdom 

R. JANSSEN 

Forschungsinstitut Senckenberg, 
Frankfurt am Main, Germany 

R. N. KILBURN 
Natal Museum 
Pietermaritzburg, South Africa 

M. A. KLAPPENBACH 

Museo Nacional de Historia Natural 

Montevideo, Uruguay 

J. KNUDSEN 

Zoologisk Institut & Museum 

Koben havn. Denmark 

A. LUCAS 

Faculté des Sciences 

Brest, France 

С MEIER-BROOK 

Tropenmedizinisches Institut 
Tübingen, Germany 



H. к. MIENIS 

Hebrew University of Jerusalem 

Israel 

J. E. MORTON 

The University 
Auckland, New Zealand 



A. STANCZYKOWSKA 
Siedlce, Poland 

F. STARMÜHLNER 

Zoologisches Institut der Universität 

Wien, Austria 



J. J. MURRAY, Jr. 
University of Virginia 
Charlottesville, U.S.A. 



Y. I. STAROBOGATOV 
Zoological Institute 
St. Petersburg, Russia 



R. NATARAJAN 

IVIarine Biological Station 

Porto Novo, India 

J. OKLAND 
University of Oslo 
Norway 

T. OKUTANI 
University of Fisheries 
Tokyo, Japan 

W. L. PARAENSE 

Instituto Oswalde Cruz, Rio de Janeiro 

Brazil 

J. J. PARODIZ 
Carnegie Museum 
Pittsburgh, U.S.A. 

J. P. POINTER 

Ecole Pratique des Hautes Etudes 

Perpignan Cedex, France 

W. F. PONDER 
Australian Museum 
Sydney 

Ol Z. Y. 

Academia Sinica 

Qingdao, People 's Republic of China 



W. STREIFE 
Université de Caen 
France 

J. STUARDO 
Universidad de Chile 
Valparaiso 

S. TILLER 

Muséum National d'Histoire Naturelle 
Pans, France 

R. D. TURNER 
Harvard University 
Cambridge, Mass., U.S.A. 

J.A.M. VAN DEN BIGGELAAR 
University of Utrecht 
The Netherlands 

J. A. VAN EEDEN 
Potchefstroom University 
South Africa 

N. H. VERDONK 
Rijksuniversiteit 
Utrecht, Netherlands 



D. G. REID 

The Natural History Museum 

London, United Kingdom 

N. W. RUNHAM 

University College of North Wales 

Bangor, United Kingdom 



B. R. WILSON 

Dept. Conservation and Land Management 

Kallaroo, Western Australia 

H. ZEISSLER 
Leipzig, Germany 



S. G. SEGERSTRLE 
Institute of Marine Research 
Helsinki, Finland 



A. ZILCH 

Forschungsinstitut Senckenberg 

Frankfurt am Main, Germany 



MALACOLOGIA, 1995, 37(1): 1-11 

THE LIFE CYCLE, DEMOGRAPHIC ANALYSIS, GROWTH AND 

SECONDARY PRODUCTION OF THE SNAIL HEUCELLA (XEROTHRACIA) 

PAPPI (SCHUTT, 1962) (GASTROPODA PULMONATA) 

IN E. MACEDONIA (GREECE). 

M. Lazaridou-Dimitriadou 

Laboratory of Zoology, School of Biology, Faculty of Sciences, Aristotle University of 
Thessaloniki, 54006 Thessaloniki, Macedonia, Greece 

ABSTRACT 

The life cycle, population dynamics, and growth of the pulmonate snail Helicella p<erothracia} 
pappi were studied in northern Greece. The spatial distribution of H. pappi was found to be 
contagious. Demographic analysis of its population revealed that (a) three cohorts exist 
throughout the year, (b) increased growth rate is observed during spring, (c) snails attain their 
maturity 21 months after hatching when their greatest shell diameter reaches 15 mm, and (d) 
it is an iteroparous species, with egg-laying in autumn. Von Bertalanffy analysis showed that H. 
pappi may reach its maximum size (dead shells collected in the field had 25.5 mm maximum 
shell diameter) in four years. Shell morphology changes when spermatozoa are fully formed in 
the gonad for the first time. Mortality rate is high just after hatching and also after winter, when 
tissue degrowth occurs, at which time the snails lose 33% of their biomass. Life expectancy 
decreases with increasing age. Net reproductive rate (Ro) was 3.025, per capita rate of increase 
(r) is 0.04, annual production (P) was 5.82 ± 0.45 g^m^-yr) in 1987 and 3.73 + 0.31 g/{vr\^-yr) in 
1988, mean standing crop (B) was 2.89 g/m^ in 1987 and 1.81 g/m^ in 1988, and annual 
productivity rate constant (P/B) was 0.2 per year in both 1987 and 1988. 

Key words: Biology, ecology, growth, production, snail, Helicella pappi, Xerolenta obvia. 



INTRODUCTION 

Little Is known about the species Helicella 
(Xerothracia) pappi Schutt, 1962. Wagner 
(1927) referred population of this species 
from near our study area in Xanthi, southern 
Thrace, to Martha filimargo Krynicki, placing 
it in the genus Helicopsis Fitzinger, 1833. Ur- 
banski (1960) said that samples from south- 
ern Thrace of Helicella (Helicopsis) filimargo 
(Rossmässler) did not differ from samples of 
Krimea and Odesco. Schutt (1962) described 
the shell and genital apparatus of samples of 
Helicella (Xerothracia) pappi from a type lo- 
cality in Philippi, Kavala, eastern Macedonia; 
he claimed that this species could not be 
placed in the genus Helicopsis, as Wagner 
(1927) had done, because of such shell fea- 
tures as curvature and the presence of a keel. 
Hausdorf (1988) claimed that /-/. pappi could 
not be placed in a subgenus of Helicella be- 
cause it differs in the dart sac and in the 
nerves coming from the cerebral ganglia. He 
concluded that it is a subspecies oi Xerolenta 
obvia. 

In the present study we are using the name 
Helicella (Xerothracia) pappi following Schutt 



(1962), because the samples come from the 
type locality. We have studied the biology 
and ecology of this species, which is re- 
stricted to Philippi, eastern Macedonia, in or- 
der to find out why this species does not 
have a broader and continuous distribution 
from Krimea to Greece. 



METHODS AND MATERIALS 

Helicella pappi was studied in the archae- 
ological site of Philippi, 25 km from Kavala, 
eastern Macedonia, Greece. Philippi is a 
limestone area with limited vegetation, in- 
cluding mosses, lichens, several Taraxacum 
species, and succulent plants. Several grass 
species are dominant. Apart from H. pappi, 
there are small, sparse populations of Lindol- 
holmia lens and Helix figulina. Weather con- 
ditions during the investigation period are 
shown in Figure 1. 

Random samples (Lewis & Taylor, 1972) 
were taken every month for three consecutive 
years between April 1986 and April 1989. No 
samples were taken in winter (December 
through February), when the snails are in di- 



U\ZARIDOU-DIMtTRIADOU 




A86M J JASON DM87 A M J J A S О N M88 A M J J A S О N D M89 A M 

Months 

FIG. 1 . Ombrothermic curve showing mean monthly temperatures (-C) and total monthly precipitation (mm) 
at Philippi from April 1986 to May 1989 (striated areas represent arid periods of the year). 



apause and hidden under vegetation. Quadrat 
sample-size (25 x 25 cm^) was determined by 
Healy's method (Cancela da Fonseca, 1965). 
Elliot's (1971) method was used to determine 
the necessary total number of sampling units 
(sampling error less than 20%). Sampling was 
carried out during morning hours in the ab- 
sence of rain. All snails found in a quadrat 
were collected, measured and then replaced. 
The largest diameter of the shell (D) and the 
peristome diameter (d) were measured with 
vernier calipers to the nearest 0.1 mm. D was 
used for size-frequency histograms, using 
3-mm class intervals (Cancela da Fonseca, 
1965). The cohorts were discriminated using 
probability paper (Harding, 1949). This 
method was valid because the modes of the 
age-classes were separated by at least 2.5 
standard deviations (Grant, 1989), except for 
two cases, one in March 1 987 and one in June 
1988; although many age classes had less 
than 50 individuals, the modal values were 
consistent from month to month. This con- 
firms that the modes were real and not the 
result of sampling variation. The same method 
has been used before for demographic anal- 
yses of other populations of molluscs 
(Hughes, 1970; Lévêque, 1972; Daguzan, 
1975; Lazaridou-Dimitriadou et Kattoulas, 
1991). 

There were no statistically significant vari- 
ations in field density over the three years. 
Life data and rate estimates were based on 
successive samples over 1987 and 1988. 

Spatial distribution of the snails in the hab- 



itat was examined by using Taylor's (1961) 
power law a^ = ax'^, where ü^ = variance and 
X = mean number of snails/0.25 m^. 

For the study of relative growth, the mor- 
phometric criteria of shell diameter (D) in re- 
lation to the peristome diameter (d) were 
used from all the animals sampled during 
1987 (N = 2567). Mayrat's method (1965a, b) 
was used to compare the growth of D in re- 
lation to d between immature and mature 
snails. A logarithmic transformation was ap- 
plied to the data. 

Bertalanffy's (1938) method was used to 
calculate the theoretical growth curve and life 
span; this method is widely used (Moreteau, 
1987). 

Life-table and fertility data, as well as an- 
nual secondary production, were estimated 
as described for Helix lucorum (Staikou et al., 
1988) and Eobania vermiculata (Lazaridou- 
Dimitriadou & Kattoulas, 1991). Annual pro- 
duction is calculated by the size-frequency 
method because single cohorts need not be 
identified. 

For dry body-weight (Wb) analysis, 1 00 an- 
imals comprising five from each size class 
were individually marked and their greatest 
shell diameter (D) was measured; they were 
then dried to constant weight over a period of 
36 h in a vacuum at room temperature. Shell 
organic matter was calculated as the residual 
weight of dry shell after treatment with 5 m 
mol/ml HCl, successive washing over a fine 
filter; the residue was dried in a vacuum. Two 
size classes were used; one comprised im- 



BIOLOGY AND ECOLOGY OF HEUCELLA PAPPI 



N/2500 cm 



30 



20- 



10 



egglaying 



T 



i 



i 



egglaying 



egglaying 



i 






П 



^1 






T 



i 



J4^ 

A 86 M J J ONDM87AMJ J AS ONM88AMJ J AS N DM 89 M 

Months 

FIG. 2. Density of Helicella (Xerothracia) pappi (number of snails/2500 cm^ (mean ± SD)) at Philippi from 
April 1986 to May 1989. Double lines on the x-axis indicate periods during which no samples were taken. 



mature snails (4 < D < 13 mm) with shell or- 
ganic matter containing 1.4% of the total 
shell weight, and the other comprised mature 
snails (14 < D < 21 mm) with shell organic 
matter containing 0.19% of the total shell 
weight. These size classes were chosen as a 
result of study of the maturation of the geni- 
talia and gonad. The shell organic matter was 
then added to the dry body weight of the 
different size classes and the sum was used 
(Table 3) in estimating annual secondary pro- 
duction. 



RESULTS 

Aspects of the Biology of Helicella pappi 

Helicella pappi is an iteroparous species 
with overlapping generations throughout the 
year. Rate of growth and reproduction were 
not constant during the three study years 
(Figs. 2, 4). The greatest shell diameter of 
sexually mature snails was 22 mm, and ma- 
turity was attained 21 months after hatching 
(Figs. 3, 4) for 98% of the population. The 
aperture lip started to form 23 to 24 months 
after hatching. In the third year, the other 2% 
of the population matured. Egg laying took 



place at the end of September, October or 
November (Fig. 2), depending on the prevail- 
ing climatic conditions, especially precipita- 
tion (Fig. 1). Measurements of ten egg 
clutches in the field showed that the mean 
number of eggs laid was 69 ± 4.3 (m ± SE), 
with a range of 42 to 85 eggs, and the mean 
weight of 70 eggs was 0.03 ± 0.004 g. The 
mean number of eggs laid by older adults, 
which had already laid eggs in the previous 
year, was 22 ± 1 .9 (m ± SE) (N = 5), with a 
range of 18 to 28 eggs. Hatching took place 
25 days to one month later, but hatchlings 
remained in the soil. The greatest shell diam- 
eter of the newly hatched snails was 1 .5 ± 
0.09 mm. By marking ten different egg 
clutches, hatching and after-hatching losses 
were estimated at 55%. After-hatching 
losses were estimated in the laboratory to be 
20%. During winter, from the end of Novem- 
ber to the end of February, the snails did not 
really hibernate. Juveniles formed a thin, 
transparent epiphragm, whereas 30% of the 
snails with 14 > D > 7 formed a thick epi- 
phragm. Snails with D > 14 mm did not form 
an epiphragm, but they diapaused under 
creeping plants occurring on the soil or 
stones. No real aestivation took place. During 
July and August, all snails diapaused during 



LAZARIDOU-DIMITRIADOU 



TABLE 1 . Estimation of statistical parameters of the population of Helicella pappi (where a, b 
= constants, r = correlation coefficient, N = number of snails examined, logd ± о.^д^ and 
logD ± OiogD = means of the greatest shell diameter (mm)(D) and the peristome diameter 
(mm)(d) ± SD)). 



Entire sample 



Juveniles 2<D<14 



Adults 14<D<22 



a±Oa 
btOb 

r2 

logd ± G,„gö 
logD ± GiogD 
N 



1.189 ±0.005 
0.302 ± 0.003 

0.954 
0.603 ±0.153 
1.019±0.182 

2569 



1.254 ±0.088 
0.270 ±0.005 

0.922 
0.515 ±0.153 
0.916 ±0.122 

1600 



0.859 ±0.012 
0.545 ± 0.009 

0.801 

0.75 ±0.057 

1.1910.049 

969 



dry weather, as in summer 1986 (Fig. 1), but 
only the juveniles formed a thin, transparent 
epiphragm. Snails were active during spring 
and on humid weather in summer (Fig. 1). 

Helicella pappi became mature and the 
genitalia became well formed when D > 14 
mm. Histologically, the gonad of these snails 
showed fully formed spermatozoa during Oc- 
tober (the reproductive period), although 
oocytes were not fully grown. There was a 
positive correlation (r^ = 0.918, N = 100, P < 
0.001) between (a) the greatest shell diameter 
(D) and the corresponding dry body weight 
and (b) the dry body weight and the dry shell 
weight (r^ = 0.742, N = 100, P < 0.001). 



4); (b) increased growth rate was observed 
during spring. An ANOVA test showed no 
statistical differences in the daily rate of 
spring growth among the three consecutive 
years of study (Fig. 4); (c) mature snails of 15 
mm attained their maximum size 21 months 
after hatching; (d) when egg laying took place 
in October (Fig. 2: 1987), depending on the 
degree of precipitation (Fig. 1), the hatchlings 
appeared in November (Fig. 3: 27-11-87). 
When egg laying took place in November, the 
hatchlings appeared in early spring (Fig. 3: 
20-3-88 and 31-3-89), possibly because it is 
safer for thin-shelled juveniles to stay buried 
in the soil. 



Population Dynamics and Spatial 
Distribution 

The population fluctuated during the study 
period (Fig. 2). The mean population density 
was 18.1 ± 3.3 snails/0.25 m^ (mean ± SE) in 
1986, 14.4 ± 6.6 in 1987, and 12.7 ± 1.5 in 
1988. An ANOVA test among the three con- 
secutive years did not show any statistical 
differences (F = 1.646, P = 0.2077) in the 
population densities. Densities of H. pappi 
peaked in early spring. The population den- 
sity was above the mean density for 5-6 
months (Fig. 2). The spatial distribution of H. 
pappi was found to be contagious because 
parameter b of Taylor's power law was equal 
to 2.043 [g'' = 1.111 (xf°^% 

Demographic Analysis of the Population of 
Helicella pappi 

The analysis of size frequency histograms 
(Fig. 3, 4) with probability paper showed that: 
(a) three cohorts existed in the habitat 
throughout the year; a fourth was added after 
the reproductive period, though the third co- 
hort contained adults of different ages (Fig. 



Relative Growth of D in Relation to d 

In the field, growth rate was high during 
periods of suitable weather, but there was no 
significant growth during winter and summer. 
Growth was most rapid in spring, from March 
till May (Fig. 4). There was a positive correla- 
tion between greatest shell diameter and peri- 
stome diameter for the whole population of 
H. pappi (Table 1). Growth rate was faster in 
juveniles (a = 1 .254) than in adults (a = 0.859), 
and growth was more heterogenous in juve- 
niles than in adults, because their standard 
deviations of the mean were greater (Table 1 ). 
According to Mayrat's (1965a, b) method, the 
intersection point between the rate growth of 
these two subpopulations Quveniles + adults) 
occurred at D = 13.9 mm. This, according to 
histological examination of gonads in relation 
to the age of the snails, was the diameter at 
which spermatozoa were fully grown. 

Absolute Growth 

The growth pattern of H. pappi seems to 
conform to the equation D, = D^ax 
[1-е ''<* '°*], which was given by D„^^^ = 



> 40 3/4/86 

30- 



20 
10- 




BIOLOGY AND ECOLOGY OF HELICELLA PAPPI 

30-, 20-, , 20 

20- 



10- 



Tffh ... mm . 0- 



^ 



25/3/87 



10- 



lh"h-rfTk> r7 0. 



24/10/87 



пШ 



10 



Д-г^ 0. 



^ 



Ышк 



1 6 12 18 1 

30 -, 8/5/86 20 -, 

20- 

10 



J 



tfUîTMfln. 



¡m 



Ьк. 



22 I 

30-, 

20- 

10- 





I , гП i n та =С 



_Ь» о I ,^ л 



10 20 

29/9/88 



1 6 12 19 ' У 

12-, 
10- п 28/5/87 



6- 



JU -| 


в/6/86 


20- 






10- 


Г 


" 


0- 


Г 


TKMÍtlh 



ш^ 



40 
30 
20 
10- 



20 1 

20^ 



ШЬо. 



гГПТЬ 



^^ 



шИПы 



1 6 12 19 



'^Т 30/6/87 
10- 



Л 



ЫЫъИЛ 



20 1 

30 

20 
h 10 

3- О, 



JlíÍMHfTIb 





1 


10 


20 


20-, 


8/12/88 


10- 

0- 


^^- 


M 


-Л 



^ 



14 21 ' 

15-, 



20 



ша-оШа 



It- 



ы 



L 



20-, 
10. 




31/3/89 


0. : 


Iff 


llHíhi 



^ 



IM^;: 



14 21 1 

20. 



^ 



tu 0. 



тЖ 



од] 



0. 





1 


10 20 


1 7 


14 21 


1 


9 


19 


20-, 
10- 


4/12/86 


12-, 
10- 

-1 ^" 

6- 


30/9/87 


15- 
-] 10- 


26/7/8 


9 




0- 


^^^--- 


4- 

iKhiTh о' 


a-^.-- 


-| 5- 

:L .: 


^^---. 


"HT 





1 10 20 ' 7 14 21 1 9 19 

D mm 

FIG. 3. Size-frequency histograms of the population of Helicella pappi at Philippi from April 1986 to May 
1989. 



28.8[1-e °°^^<'"°-2'^']. According to this 
method, the greatest shell diameter mea- 
sured in the field (inferred from dead shells (D 
= 25.6 mm)) may be attained in 48 months. 
The above equation was calculated by using 



the known greatest shell diameter in the field 
(26 mm), the mean D value of newly hatched 
snails, which was 1 .2 mm, and the mean size 
of young snails first sampled in the field, 
which was 1.5 mm (Fig. 3: November 1987). 



6 

30 



LAZARIDOU-DIMITRIADOU 



20 



Dmm 




// 1 ■ 1 ' 

s N M. 88 A 


M J 


— 1 — ■— 1— 1 

J л 


s 


о 


N 


1 // 1 ■ 1 
D M. 89 A 


Months 















A. 86 M J J 



S О N D M. 87 A M J J 



FIG. 4. Modal distribution of Helicella pappi at Philippi from April 1986 to May 1989. Broken lines indicate 
periods during which no samples were taken. Gi-Gg indicate the different generations during the study 
period. Time breaks denote winter time, during which diapause took place and no samples were taken. 



Dt is the shell diameter at time t; D^na^ is the 
diameter at the upper growth asymptote cal- 
culated according to Ford-Walford equation 
(Walford, 1946); t is time in months, tg is the 
hypothetical time when D is equal to zero (mi- 
nus the egg stage for this paper), and к is the 
growth rate coefficient. 



Life and Fertility Table 

For the construction of the fertility table, 
we used (a) the numbers of eggs laid by two 
or three-year old adults, and by adults of 
more than three years old, known from field 
observations and (b) egg-hatching and after- 
hatching losses calculated in the field and the 
laboratory respectively. 

From Table 2, the following may be con- 
cluded: (a) mortality rate (Kx) was high after 
hatching and then stabilized. It increased af- 
ter the first winter, before the second winter 
(in 3-year-old adults snails) and stayed high 
after the third winter, (b) values of expecta- 
tion of life (ex) decreased with increasing age, 
(c) the value of net reproductive rate (Ro) was 
high (Ro = 3.024), and (d) the per capita rate 
of increase was greater than zero, with a rate 
of 0.04 per unit of time. 



Annual Secondary Production 

The calculations for Hynes' size-frequency 
method are listed in Table 3. The mean bio- 
mass of each size class was expressed as 
dry-weight of body plus organic material of 
the shell. After conversion, using Benke's 
(1979) correction, annual production (P) was 
found to be 5.82 ± 0.45 g^m^-yr) in 1987 and 
3.73 ± 0.31 g/(m2-yr) in 1988. Biomass (B) 
was 2.89 g/m^ in 1 987 and 1 .81 g/m^ in 1 988. 
The annual productivity rate constant (P/B) 
was 0.21 in both 1987 and in 1988. Turnover 
time (B/P X 365 days) was 1765 days in 1987 
and 1775 days in 1988. 



DISCUSSION 

The contagious spatial distribution of H. 
pappi is similar to the xerothermophilic spe- 
cies living in similar habitats in Greece (e.g., 
Xeropicta arenosa and Cernuella virgata (Laz- 
aridou-Dimitriadou & Kattoulas, 1985). 

Recruitment of newly hatched snails of H. 
pappi seems to be the main reason for the 
rise in population density after winter. The 
low values of population density in November 
and December are due to the fact that some 



BIOLOGY AND ECOLOGY OF HELICELLA PAPPI 

TABLE 2. Life and fertility table of a cohort of Helicella (Xerothracia) pappi starting in April 
1986 (Figure 3-G3). 



Age 














(months) 


L 


Qx 


К 


Sx 


ГПх 


Lxm, 


1 


1000 


0.27 


0.31 


12.29 


0.00 


0.00 


2 


730 


0.00 


0.00 


15.65 


0.00 


0.00 


3 


730 


0.00 


0.00 


14.65 


0.00 


0.00 


4 


730 


0.00 


0.00 


13.65 


0.00 


00 


5 


730 


0.18 


0.20 


12.65 


0.00 


0.00 


6 


600 


0.00 


0.00 


14.28 


0.00 


0.00 


7 


600 


0.06 


0.06 


13.28 


0.00 


0.00 


8 


565 


0.00 


0.00 


13.07 


0.00 


0.00 


9 


565 


0.00 


0.00 


12.07 


0.00 


0.00 


10 


565 


0.01 


0.01 


11.07 


0.00 


0.00 


11 


560 


0.00 


0.00 


10.14 


0.00 


0.00 


12 


560 


0.39 


0.47 


9.14 


0.00 


0.00 


13 


350 


0.00 


0.00 


13.32 


0.00 


0.00 


14 


350 


0.00 


0.00 


12.32 


0.00 


0.00 


15 


350 


0.00 


0.00 


11.32 


0.00 


0.00 


16 


350 


0.00 


0.00 


10.32 


0.00 


0.00 


17 


350 


0.00 


0.00 


9.32 


0.00 


0.00 


18 


350 


0.00 


0.00 


8.32 


0.00 


0.00 


19 


350 


0.01 


0.01 


7.32 


0.00 


0.00 


20 


347 


0.63 


0.98 


6.39 


0.00 


0.00 


21 


130 


0.00 


0.00 


15.25 


0.00 


0.00 


22 


130 


0.00 


0.00 


14.25 


0.00 


0.00 


23 


130 


0.00 


0.00 


13.25 


18.00 


53.75 


24 


130 


0.14 


0.15 


12.25 


0.00 


0.00 


25 


112 


0.00 


0.00 


13.09 


0.00 


0.00 


26 


112 


0.00 


0.00 


12.09 


0,00 


0.00 


27 


112 


0.00 


0.00 


11.09 


0.00 


0.00 


28 


112 


0.03 


0.03 


10.08 


0.00 


0.00 


29 


110 


0.00 


0.00 


9.40 


0.00 


0.00 


30 


110 


0.00 


0.00 


8.40 


0.00 


0.00 


31 


110 


0.00 


0.00 


7.40 


0.00 


0.00 


32 


110 


0.10 


0.10 


6.40 


0.00 


0.00 


33 


101 


0.00 


0.00 


6.03 


0.00 


0.00 


34 


101 


0.00 


0.00 


5.03 


0.00 


0.00 


35 


101 


0.07 


0.07 


4.03 


7.00 


24.07 


36 


90 


0.15 


0.17 


3.30 


0.00 


0.00 


37 


77 


0.27 


0.32 


2.81 


0.00 


0.00 


38 


56 


0.19 


0.21 


2.67 


0.00 


0.00 


39 


46 


0.38 


0.49 


2.18 


0.00 


0.00 


40 


28 


0.38 


0.47 


2.22 


0.00 


0.00 


41 


18 


0.40 


0.51 


2.26 


0.00 


0.00 


42 


10 


0.33 


0.41 


2.43 


0.00 


0.00 


43 


7 


0.00 


0.00 


2.40 


0.00 


0.00 


44 


7 


0.50 


0.69 


1.40 


0.00 


0.00 


45 


4 


0.50 


0.69 


1.30 


0.00 


0.00 


46 


2 


0.60 


0.92 


1.10 


0.00 


0.00 


47 


1 


0.50 


0.69 


1.00 


0.00 


0.00 


48 





1.00 


0.00 


0.50 


0.00 


0.00 


Ro = XL^m^ 


= 3.025 r = 


InRo / Tc = 


0.04 









1^ : Number of animals surviving at the beginning of age-class x (months) out of 1,000 originally hatched, 
q^ : Mortality rate during age interval x (d^/l^, where d>, is the number of animals during age interval x). 
K^ : Intensity or rate of mortality: loga^ - loga^ ^. 

e^ : Expectation of life: JJ\^ where T^ = L^ + Ц i L^ (Ц : is the number of animals alive between age 

X and x+1: (!>< + 1^ i)/2; L^, is the total number of animals x age units beyond age x). 

L^m^ : Total number of hatchlings in each age interval (m^ : Number of living animals hatched per adult 

snail). 

where Ro is net reproductive rate, r is per capita rate of increase, and Tc is generation time (25,7 months). 



8 



LAZARIDOU-DIMITRIADOU 



TABLE 3. Calculation of production of Helicella pappi by the size-frequency method. Annual production 
based on sets of samples from Apnl 1988 to April 1989 (where ñ, = number of snails at the size class j 
in number; Uñ| = variance of п,; W, = mean individual dry body weight + mean dry shell of organic 
matter (in mg); G, = geometric mean of weight of pairs of successive size classes; В = mean standing 
crop or population biomass in mg; P = annual production in mg; P/B = annual turnover ratio; a = 
number of size classes; CPI = cohort production interval: 730 days). 















(B> 


P' 


Class 






n, 


W, (mg) 


_- G, 


[ñjWj] 


(n,ñ,,,)(G,) 


range 


П| /0.25m' 


' Un, 


n,.i 


± St. error 


(W,W,,,)°' 


(mg/0.25 m^) 


(mg/0.25 m^) 


1-2 


0.01 


0.0000 


-0.13 


0.410 ±0.01 


0.41 


0.0051 


-0.0549 


2-3 


0.15 


0.0020 


-0.35 


0.410 ±0.02 


0.64 


0.0600 


-0.2258 


3-4 


0.50 


0.0554 


-0.22 


1.000 ±0.02 


1.00 


0.4990 


-0.2233 


4-5 


0.72 


0.1764 


-0.05 


1.000 ±0.03 


1.41 


0.7223 


-0.0738 


5-6 


0.77 


0.0806 


-0.25 


2.000 ±0.14 


3.16 


1.5489 


-0.7781 


6-7 


1.02 


0.0960 


-0.46 


5.000 ±0.27 


5.92 


5.1025 


-2.7369 


7-8 


1.48 


0.2454 


0.12 


7.000 ±1.00 


7.48 


10.3819 


0.9115 


8-9 


1.36 


0.2364 


0.37 


8.000 ± 0.44 


9.38 


10.8906 


3.5145 


9-10 


0.99 


0.0892 


0.04 


11.000 ±1.00 


12.85 


10.8534 


0.5313 


10-11 


0.95 


0.0828 


0.39 


15.000 ±1.00 


18.17 


14.1796 


7.0363 


11-12 


0.56 


0.0493 


-0.06 


22.000 ± 3.00 


23.92 


12.2754 


-1.3548 


12-13 


0.61 


0.0436 


0.07 


26.000 ± 2.00 


26.50 


15.9802 


1.9403 


13-14 


0.54 


0.0483 


-0.15 


27.000 ±4.00 


31.18 


14.6175 


-4.7975 


14-15 


0.70 


0.0616 


-0.23 


36.000 ± 2.00 


42.00 


25.0296 


-9.7470 


15-16 


0.93 


0.0980 


0.10 


49.000 ±2.00 


49.99 


45.4396 


4.9246 - 


16-17 


0.83 


0.0677 


-0.07 


51.000 ±2.00 


57.58 


42.2702 


-4.2654 


17-18 


0.90 


0.0736 


0.37 


65.000 ± 4.00 


67.93 


58.6892 


25.1060 


18-19 


0.53 


0.0427 


0.37 


71.000 ±5.00 


77.69 


37.8676 


28.9068 


19-20 


0.16 


0.0058 


0.15 


85.000 ± 5.50 


106.72 


13.7058 


16.0344 


20-21 


0.01 


0.0003 


0.01 


134.000 ±6.00 


134.00 


1.4744 


1 .4744 




13.73 


X 4 = 


321 .593 


x4 = 


66.1227x4 = 




54.92/m2 


(259 days) 






1286.36 mg/m^ (259d) 


264.49 mg/m^ (259 d) 




77.39/m2 


(365 days) 






1812.82 (365 d) 


372.74 (365 d) 



P = 20 X 365/730 X 372.74 = 3727.4 mg/(m2.yr) or or 3,727 g/(m2.yr) 

U(P) = Uñ,(G, G, i)2 X a^ X (365/730) = 24371 .67 

2[U(P)°=] = (24371. 67)° s = 312.22 = 0.31 

P = 3.73 ± 0.31 g/(m2.yr) 

P/B = 372.74/1812.82 = 0.206 

Turnover time = B/P x 365 = 1 775.2 days 



snails are already dormant because of the 
prevailing weather conditions and the fact 
that old adults and some new adults (D > 15 
mm) die after egg laying. The population dy- 
namics suggests that there is a characteristic 
annual periodicity, with synchronization of 
population and life-cycle development. This 
appears to be a species adapted to recover 
slowly after an adverse period. The slow re- 
covery of the population results from the low 
hatch-rate of eggs deposited just before the 
adverse period. The low rate of juvenile de- 
velopment into adult stage during spring, and 
the rapid decline in population size after the 
density peak, indicate a reduced reproduc- 
tive effort of later adult stages. 

increased growth took place during spring 
because temperatures were not exceedingly 
high (20°C), and total monthly precipitation 



did not fall below 20-30 mm (Fig. 1). During 
autumn, growth took place only in juveniles 
(Fig. 4) when temperatures were around 1 5°C 
(in October and November) and only if there 
was precipitation. Newly hatched snails dur- 
ing that period of the year remained dormant. 
The rate of growth, however, was not the 
same for newly hatched snails and juveniles 
(Fig. 4). This is also related to differences in 
temperature [e.g., the 1987 March (5.8") and 
April (12.5 ) temperatures were lower than in 
1986 (8.6 - 15.4 С respectively)]. Addition- 
ally, the growth rate was not the same for 
juveniles and mature snails. This was evident 
from the study of the population analysis of 
H. pappi and from the comparison of the rate 
of relative growth of D in relation to d be- 
tween juveniles and adults. This is a general 
phenomenon in many Helicidae and it is usu- 



BIOLOGY AND ECOLOGY OF HELICELLA PAPPI 



ally due to internal changes in genitalia and 
gonad maturation (Yom-Tov, 1971; Bonavita, 
1972; Williamson, 1976; Lazaridou-Dimitria- 
dou, 1986; Staikou et al., 1988). Seasonal 
variation in growth and, more specifically, in- 
creased growth rate in spring, have been re- 
ported for other snails in Greece, including E. 
vermiculata (Lazahdou-Dimitriadou & Kattou- 
las, 1985), X. arenosa and С virgata (Lazah- 
dou-Dimitriadou, 1986), H. lucorum (Staikou 
et al., 1988), В. fruticum (Staikou et al., 1990), 
and M. cartusiana (Staikou & Lazaridou-Dim- 
ithadou, 1990). Baba (1985) also reports that 
growth is related to climatic factors and that 
it increases only before sexual maturity. As 
for H. lucorum (Staikou et al., 1988), ß. fruti- 
cum (Staikou et al., 1990) and other terrestrial 
snails, H. pappi continues to increase D even 
after maturation, because it is heterothermic. 
There were adverse periods during which ac- 
tivity, and consequently growth and repro- 
duction, stopped. These periods coincided 
mainly with winter and summer drought. 
Moreover, the values of к showed that winter 
constitutes the most important environmen- 
tal stress. Helicella pappi matures only in the 
second year of its life, with a rate of increase 
equal to 0.041. Being iteroparous, this snail 
reproduces again after its first egglaying. 
However, it seems that high reproductive 
output on one occasion influences future re- 
productive output. Although Ro and the turn- 
over time was high (1 ,775 days), productivity 
rate (0.2/year) was low, which may be related 
to the long life span (4 years) and high mor- 
tality of this species at subadult and adult 
stages, especially after winter. Moreover, 
maintenance costs during dormant periods 
are increased; 33% of the previously ac- 
quired biomass is lost. These snails try to ex- 
ploit favourable conditions, but the absence 
of a true hibernation or aestivation and a var- 
ied capacity for dormancy cause the death of 
much of the population. The annual adult 
mortality rate was similar to that reported by 
Osterhoff (1977) and Williamson et al. (1977) 
for С. nemoralis and by Shachak et al. (1975) 
for Spliincterochila zonata, which also has a 
life-span of 4-6 years. Turnover times are ob- 
viously related to length of life; long turnover 
times have only been reported for such bi- 
valves as Anodonta (1,789 days/4.9 years) 
(Russell-Hunter & Buckley, 1983) and for the 
terrestrial snail Monaclia (1,177 days/2-3 
years) (Staikou & Lazahdou-Dimitriadou, 
1990). Otherwise, terrestrial snails seem to 
have short turnover times from 50.7 days 



(Vallonia, Russell-Hunter & Buckley, 1983) to 
293 days/3 years (Helix lucorum, Staikou et 
al., 1988). However, the possibility of long 
turnover times in age-structured populations, 
especially in relation to interspecific compar- 
isons, must be treated with caution, because 
some average standing-crop values in the lit- 
erature are estimated from an entire popula- 
tion and others from a model cohort. Gener- 
ally, turnover times of more than two years 
appear to be associated with life spans of 
four years or more. The fact that H. pappi has 
long turnover times and a low productivity 
rate may be related to its small size, its long 
life span, and the fact that it is iteroparous. 
Published distribution data seem to sug- 
gest that H. pappi comprises a species with a 
patchy disthbution (Schutt, 1 962). Because of 
its evolutionary origin in colder climates (Ur- 
banski, 1960), this species manages barely 
to survive in this region of Greece, with wide 
daily and seasonal temperature variations. 
Actually, it is the climatic factors that play an 
important role in controlling energy flux in H. 
pappi. Low rates and efficiencies of growth 
place severe restraints on the snail's ability to 
meet the demands of over-winter mainte- 
nance and reproduction. As a result, repro- 
duction is delayed until the second autumn. 
Energy investment is not concentrated on egg 
production, and there is variation in rates of 
growth and fecundity according to age. Mor- 
tality takes place at all stages, but mainly after 
winter; high mortality after adverse periods of 
the year is a common characteristic of many 
helicid snails. Consequently, the demograph- 
ic characteristics of Helicella conform to an 
A-selectionist's strategy, as defined by Green- 
slade (1983); that is, suitable conditions for 
breeding last for only a short period but occur 
regularly and predictably, such that the pop- 
ulation synchronizes with those conditions 
(Figs. 1, 2). Moreover, interspecific competi- 
tion is rare, because only very small, sparse 
populations of Lindolhomia lens and Helix 
figulina were observed. 



ACKNOWLEDGEMENTS 

I would like to thank Dr. E. Gittenberger of 
The Natural Museum of Leiden for informa- 
tion on the distribution and systematic posi- 
tion of Helicella (Xerothracia) pappi. Thanks 
are also due to Dr. G. B. J. Dussart from 
Christ Church College, Canterbury, U.K, for 
his critical remarks, K. Asmi and Dr. A. 



10 



LAZARIDOU-DIMITRIADOU 



Staikou for their technical help, and Dr. T. 
Sofianidou for providing me with samples 
from the area of Philippi before this study 
was undertaken. 



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Revised ms. accepted 28 November 1994 



MALACOLOGIA, 1995, 37(1): 13-21 

EGG-LAYING AND ASSOCIATED BEHAVIOURAL RESPONSES OF 

LYMNAEA PEREGRA (MÜLLER) AND LYMNAEA STAGNALIS (L.) 

TO CALCIUM IN THEIR ENVIRONMENT 

Hilary Piggott & Georges Dussart 
Canterbury Christ Church College, Canterbury, Kent CT1 1QU, United Kingdom 

ABSTRACT 

In laboratory trials, specimens of the freshwater pulmonate snail Lymnaea peregra from 
Ullswater, a soft-water lake in the English Lake District (6.5 mg/l [Ca^*], pH 7.1), showed a 
significant preference for laying eggs on clean, dead conspecific snail shells (x^ = 38.91, P < 
0.001 n = 20), thereby confirming anecdotal field observations of this behaviour. 

A choice chamber was used to investigate to test the hypothesis that lymnaeid snails might 
be able to use calcium as a cue for orientation, for example as a stimulus to find target shells 
for oviposition. Lymnaea stagnalis showed a more positive response to calcium than did L. 
peregra (t = 4.2, P < 0.05, n = 137). When snails from soft-water environments were reared in 
soft water in the laboratory, specimens of L. peregra showed a strong preference for calcium 
(X^ = 19.6, P < 0.001, n = 202), but specimens reared in hard water (84 mg/l [Ca^*], n = 44)) 
showed no such preference. The hypothesis that snails could use a calcium cue to select a shell 
as an oviposition site was supported, and, in addition, the breadth of the chemical niche of L. 
peregra appears to be wider than that of L. stagnalis. 

Key words: egg-laying, calcium, preference, ecology, hardness, Lymnaea peregra, Lymnaea 
stagnalis. 



INTRODUCTION 

The importance of calcium in the distribu- 
tion of freshwater molluscs has been widely 
reported (Boycott, 1936; Macan, 1950; 
Okland, 1969; Williams, 1970; McKillop & 
Harrison, 1 972). In his qualitative study of the 
ecology of freshwater molluscs in Britain, 
Boycott suggested that whereas some spe- 
cies were restricted to waters with calcium 
concentration exceeding 20mg/l, other spe- 
cies were more tolerant and could occur both 
in high calcium waters and elsewhere in low 
calcium waters, L. peregra being a typical ex- 
ample of such tolerance. Boycott (1936) also 
highlighted the difficulty of separating water 
chemistry from geographical distribution and 
physical characters of the habitats. In quan- 
titative studies of molluscan ecology in rela- 
tion to water chemistry, Dussart (1976) 
showed that general mollusc abundance was 
greater in hard waters ([Ca"^] > 40 mg/l), al- 
though medium waters ([Ca^""] 5-40 mg/l) 
had greater species diversity. As well as af- 
fecting distribution, calcium concentration 
also affects such aspects of freshwater mol- 
lusc biology as shell composition in planorbid 
snails (Madsen, 1987), freshwater sphaehid 
clams (Burky et al., 1979), and the ampullariid 



snail Mansa cornuarietis (L.) (Meier-Brook, 
1978). Other evidence of a direct metabolic 
response to environmental calcium was 
demonstrated by Dussart & Kay (1980), who 
showed that L. peregra reared in waters of 
different hardness had different respiration 
rates. 

Dussart (1979) observed anecdotally that 
in some soft-water habitats, L. peregra ap- 
peared to show a preference for laying eggs 
on the shells of other L. peregra from the 
same generation, and it was proposed that 
this behaviour could possibly ". . . provide an 
immediate source of nutrients to the off- 
spring after the post-egg laying deaths of the 
parent population." These observations 
therefore raised questions about whether 
snails could behaviourally orientate to envi- 
ronmental calcium. Thomas (1982) observed 
that taxes of freshwater molluscs along inor- 
ganic ion gradients had been little studied. 
There is precedent for suggesting that fresh- 
water molluscs exhibit chemoreception, 
because, for example, the freshwater pulmo- 
nate Planobahus corneus (L.) can discrimi- 
nate between amino acids (Lombardo et al., 
1991), and Thomas et al. (1980) observed 
species-specific responses to four amino 
acids. 



13 



14 



PIGGOTT & DUSSART 



Lymnaea peregra is probably the most 
common freshwater snail in Europe (Fitter & 
Manuel, 1986); it occurs in all types of habi- 
tats, including water with a calcium concen- 
tration as low as 1 mg/l. By contrast, L. stag- 
nalis is a calciphile species comprising larger 
individuals, often sympatric with L. peregra in 
harder waters. The objectives of the following 
experiments were therefore, firstly to investi- 
gate the hypothesis that soft-water snails 
might lay eggs preferentially on the shells of 
other individuals, secondly to investigate 
whether L. peregra and L. stagnalis might ori- 
entate to calcium in solution and thirdly, to 
identify any species-specific differences in 
such behaviour. 



MATERIALS AND METHODS 

Sources and Maintenance Conditions 
of Snails 

All samples were taken in June and July 
1992, when L. peregra were obtained from 
the River Stour in Kent (OS ref. TRI 785990, 
84 mg/l [Ca^""], pH 7.4) and L. stagnalis were 
collected from Monkton Nature Reserve (OS 
ref. TR657295, 72mg/l [Ca^"], pH 7.5). Spec- 
imens of L. peregra were also collected from 
Ullswater, a soft-water lake in the Lake Dis- 
trict (OS ref. NY421205, 6.5 mg/l [Ca^"], pH 
7.1). In all the choice experiments, snails 
were young-mature specimens, of about 
8-1 1 mm maximum length for L. peregra and 
25-35 mm maximum length for L. stagnalis; 
because some of the snails came from the 
field, age could only be estimated. Other- 
wise, snails were four-six months old. 

Snails were housed in the laboratory in 
plastic tubs measuring 16x16x16 cm, each 
tub containing one litre of water and ten 
snails. Where snails from hard water were 
being cultured in hard water, water from the 
River Stour was used. The snails were main- 
tained at room temperature, with continuous 
aereation, in natural daylight and fed fresh 
lettuce every three days; ten millilitres of fil- 
tered pond water were added to each tub to 
provide additional micro-nutrients. A small 
quantity of washed, fine sand was provided 
in each tub to aid digestion, and the water 
was changed at three-day intervals. In the 
experiment to investigate substratum choice, 
two round, flint pebbles (1 mm diameter, the 
approximate size of an L. peregra shell), and 
two empty L. peregra shells were added to 



each tub. Each tub thus comprised a micro- 
cosm for which both the number of egg cap- 
sules and the area of the surface types upon 
which eggs were laid was recorded, includ- 
ing the submerged walls of the tub. 

Review of Choice-Chamber Designs for 
Aquatic Snails 

Various experimental designs have been 
employed to examine chemoreception in 
aquatic molluscs. For example, Uhazy et al. 
(1978) investigated chemicals attractant to 
Biomphalaria glabrata (Say) by using a grid of 
10x5 units marked on a white enamel dish 
with test material at one end of the dish and 
control material at the other; Madsen (1992) 
used a similar design in food location exper- 
iments for Helisoma duryi (Wetherby) and Bi- 
omphalaria camerunensis (Boettger). Lom- 
bardo et al. (1 990) used a 'Y' shaped maze to 
investigate Planorbarius corneus, whereas 
Thomas et al. (1980) used an olefactometer 
to investigate the response of B. glabrata to 
amino acids and related compounds. 

There are however, many problems asso- 
ciated with the design of such experiments; 
firstly, diffusion causes dynamic change in 
ionic concentrations, so that snails might be 
responding to an ionic flow, as opposed to 
absolute concentrations. Secondly, the ani- 
mals might become satiated as they move up 
the concentration gradient so that their be- 
haviour changes accordingly. Thirdly, there 
are problems of deciding when a choice has 
been made; for example, Lombardo et al. 
(1991) reported that a time limit was neces- 
sary due to the slowness and sometimes in- 
activity of the snails in their experiments. 
Fourthly, the distinction between olfaction 
and gustation is not clear in aquatic molluscs 
(Kohn, 1961). Fifthly, when a liquid medium 
rather than a solid object is the object of the 
choice, there are problems of experimental 
design because seiche phenomena can be 
entrained at the start of each trial. Given the 
nature of the animal, it is unlikely that any 
aquatic choice-chamber design will be 
wholly satisfactory for aquatic snails. 

To circumvent these problems, Vareille- 
Morel (1986) used a flowing water design in 
studies of the response of Potamopyrgus 
jenkinsi Smith to a nutrient source, and Dus- 
sart (1973) used a static chamber with a 
"starting box"; test specimens introduced 
into the starting box had an instant choice of 
waters when the starting gate was removed. 



RESPONSE OF LYMNAEA TO ENVIRONMENTAL CALCIUM 



15 



Central baffle 




FIG. 1. Choice chamber used in the present study. 

Design of the Choice-Chamber 

Because L. stagnalis and L. peregra can be 
amphibious, the choice-chamber shown in 
Figure 1 was used, as it circumvents many of 
the problems described above. Preliminary 
dye experiments and water samples taken 
during the trials showed that there was no 
significant transfer of chemicals across the 
central divider; the latter was made of wood 
(ramin) because streaming was found to oc- 
cur when plastic dividers were used. 

Character of Water 

For all choice experiments, solutes were 
added to distilled de-ionised water to give 
the following standard water (mg/l): magne- 
sium, 15; sodium, 30; potassium, 7; ortho- 
phosphate, 15; calcium, 0; pH 7.5; (pH ad- 
justment with 2M HCl). By contrast, the test 
hard water included 50 mg/l calcium. 

Methods of Testing Preferences 

Testing one species at a time, up to ten 
snails were placed on the divider, all facing 
the same way. They could then move to the 
left or right, or could remain on the divider. To 
prevent extraneous bias, the location of 
choice waters were systematically varied be- 
tween runs. Because Green et al. (1992) had 
shown significant anticlockwise-left move- 
ment of L. peregra when out of water, runs 
were repeated, with all the snails facing in the 
opposite direction. There were thus four ori- 
entations in each run and each run was re- 
peated, so that approximately 80 snails were 
involved in each trial. Similar numbers of 
snails were used by Madsen (1992) in food 
location experiments. After ten minutes, or 
sooner if all the snails had moved, the snails 
were removed from the choice chamber and 
the dividers cleaned; there was no contact 



between snails and no evidence of trail fol- 
lowing. 

X^ tests with Yate's corrections were used 
to see if there was a significant choice and 
snails which stayed on the central divider 
were not included in the analysis. For the final 
investigation, L. peregra reared from eggs 
produced by Ullswater snails were used. Two 
batches of adult snails were separately main- 
tained in soft water (5 mg/l [Ca^^]), and two 
batches were separately maintained in hard 
water (84 mg/l [Ca^^]), both being kept for 
1-3 weeks before the trials. 



RESULTS 

Oviposition Choice of L. peregra 

Besides the walls of the tub, the snails had 
only two pebbles and two shells upon which 
to lay, so that oviposition on these surfaces 
needed a significant positive choice. After 
correction of the data for available area, soft- 
water snails imported from Ullswater showed 
a significant bias towards laying eggs on 
shells, and this bias was greater for snails 
which, before the trials, had been kept in the 
laboratory in soft water (x^ = 38.91, P < 
0.001) compared with those kept in hard wa- 
ter (x^ = 13.49, P < 0.01). These results imply 
that L. peregra from soft water showed a 
preference for laying eggs on snail shells, 
particularly having been maintained in soft 
water. It is a statistical requirement of a chi- 
square test that no observed values should 
be less than five; because no eggs were laid 
on the pebbles, this requirement was not 
met, and the results should therefore be 
treated with caution; it is conceivable that 
eggs might never have been laid on a flint 
pebble. It should be noted that in other batch 
cultures however, eggs were intermittently 
laid on such pebbles. 

Choice Experiments 

A number of preliminary tests were con- 
ducted. Ten L. stagnalis were housed in soft 
water and used in the following preliminary 
experiments. When given a choice of sodium 
and calcium cations but with the same con- 
centrations of chloride anions, the null hy- 
pothesis could be refuted at P < 0.05, imply- 
ing that movement was significantly towards 
the source of calcium (Table 1 -Trial (i)). To 
determine whether this apparent bias was 



16 



PIGGOTT & DUSSART 



TABLE 1. Preliminary investigation of choice behaviour. For the purposes of this report, a trial is defined 
as an opportunity to make a choice by a single individual snail. Because some snails stayed on the 
central baffle for the duration of an experiment, the number of movements is frequently less than the 
number of trials. In experiments (i)-(iv), each of the ten snails was tested four times (i.e. four runs) in 
the four orientations, giving 160 trials. 

Preliminary trials — ten mature specimens of L. stagnalis previously housed in soft water for one week 

Bias Towards.. x^ Significance 



4.2 P < 0.05 



(i) Comparison of cations 










100 mg/l [CI ] 


cf 


100 mg/l [СГ] 




(as NaCI) 


(as 


Ca CI2.2H; 


2O) 




Movements 81 




56 




[Ca^1 


(ii) Sodium against water 










100 mg/l [Na*] 




cf НзО'' 






(as NaCI) 










Movements 73 




50 




[Na1 


(iii) Calcium against water 










100 mg/l [Ca^*] 




cf 




НзО'' 


(as Ca CI2.2H2O) 










Movements 89 




53 




[Ca2*] 



3.9 P < 0.05 



8.8 P < 0.01 

Osmotic Potential Trial — 40 mature specimens of L. stagnalis previously housed in soft water for one 
week were tested in each of the four orientations, i.e. 160 trials. 

Bias Towards.. x2 Significance 

(iv) [Ca^"] cf [Na"] 

500 mg/l 370 mg/l 

(as Ca CI2.2H2O) (as NaCI) 

Movements 92 45 [Ca^*] 15.4 P < 0.001 



prompted by an aversion for sodium, the 
snails were given a choice between sodium 
and de-ionised water in Trial (ii). Again, the 
null hypothesis could be refuted at P < 0.05, 
implying that the snails chose the sodium re- 
gime and aversion had not been a factor in 
Trial (i). 

In Trial (iii), there was again an apparent 
bias towards calcium, implying that the null 
hypothesis could be refuted at P < 0.01 ; this 
could represent an aversion to de-ionised 
water, possibly due to the effects of osmotic 
potential. Freshwater gastropods have body 
fluids that are hyper-osmotic to the external 
media and therefore have to cope with 
the continual influx of water. To establish 
whether the difference in osmotic pressure 
between the test substances was affecting 
the responses, in Trial (iv), snails were offered 
a choice between calcium and sodium but at 
concentrations that would each exert the 
same osmotic potential. The result provides 
evidence to refute the null hypothesis that 
there is no significant difference in the re- 
sponse of snails to different substances of 
the same osmotic pressure at P < 0.01; the 
snails apparently once again showed a sig- 
nificant bias towards the water containing 
calcium. 



To investigate whether there might be spe- 
cies-specific differences in these move- 
ments, 40 specimens each of L. stagnalis 
from Monkton and L. peregra from the Stour 
were maintained in hard and soft water for 
periods of one to three weeks before inves- 
tigation. The results of the main trials shown 
in Table 2 allow comparison between their 
behaviour. Trials (v) and (ix) were controls 
showing that when exposed to identical test 
substances, there was no significant bias in 
choice for either species. 

For Trials (vi) to (viii), L. stagnalis displayed 
a highly significant positive response to cal- 
cium, but in Trials (x) to (xii), L. peregra 
showed a lower response (Table 2). A Stu- 
dent's t-test of these data confirmed this dif- 
ference; across the three trials, the mean 
number of L. stagnalis choosing calcium was 
42.1 7 with a comparable mean of 32.42 for L. 
peregra, thereby indicating that L. stagnalis 
were orientating more strongly than L. pere- 
gra (t = 4.33). The responses for both species 
towards calcium differed, depending on the 
length of time they had been maintained in 
hard or soft water before the experiment. For 
example, the x^ value for L. stagnalis that had 
been kept in soft water for one week was 
62.3, compared with 19.5 for snails that had 



RESPONSE OF LYMNAEA TO ENVIRONMENTAL CALCIUM 



17 



TABLE 2. Results of trials to investigate choices of forty individuals of each of L. stagnalis and L. 
peregra. Snails were kept in either hard water for one week (H1), hard water for two weeks (H2), soft 
water for one week (S1) or soft water for three weeks (S3). All calcium was presented as 100 mg/l 
calcium as [Ca CI2.2H2O]. Each snail was tested twice in each of the four orientations, i.e. 320 trials. 



Trial 




Choice Available 




Result 




L. stagnalis 








Bias Towards.. 


x' 


Significance 


(V) HI 


[Ca^l 


cf 


[Ca^l 








Movements 


140 




135 


neither 


0.08 


N.S. 


(vi) H2 


[Ca^l 


cf 


H2O' 








Movements 


155 




98 


[Ca^-] 


12.4 


P < 0.001 


(vii) SI 


[Ca2l 


cf 


НзО'' 








Movements 


186 




61 


[Ca^l 


62.3 


P < 0.001 


(viii) S3 


[Ca^l 


cf 


НгО'' 








Movements 


165 




93 


[Ca^l 


19.5 


P < 0.001 


L. peregra 














(ix) HI 


[Ca^-] 


cf 


[Ca^l 








Movements 


135 




139 


neither 


0.08 


N.S. 


(X) H2 


[Ca^l 


cf 


HgO'^ 








Movements 


124 




123 


[Ca^l 





N.S. 


(xi) SI 


[Ca2l 


cf 


HjO'' 








Movements 


132 




95 


[Ca^l 


5.7 


P < 0.05 


(xii) S3 


[Ca^l 


cf 


HjO'' 








Movements 


133 




69 


[Ca^l 


19.6 


P < 0.001 



been kept in soft water for three weeks; by 
contrast, the equivalent x^ values for L. per- 
egra were 5.7 compared with 19.6. 

It is possible that the snails were orientat- 
ing to chloride rather than calcium. However, 
Trial (x) for L. peregra showed no significant 
preference between chloride and de-ionised 
water; and, in fact 34 snails compared with 
26 snails actually migrated into the de- 
ionised water. There is always the possibility, 
however, that this experiment shows a bal- 
anced preference/aversion for both chloride 
and de-ionised water. For example, aversive 
behavioural and physiological responses to 
salinity are well documented (Perkins, 1974). 
The animals may have balanced their aver- 
sion to salinity with an aversion to the os- 
motic problems posed by deionised water, 
and consequently made no significant 
choice. 

Those L. peregra that had been raised in 
hard water showed no calcium preference 
(Table 3). By contrast, L. peregra raised in 
soft water showed a significant preference 
iX^ = 8.2, P < 0.01) for calcium. For example, 
over four runs, the mean number of snails 
that had been raised in hard water and chose 
calcium was 6.5, and the mean number of 
snails that had been raised in soft water and 
chose calcium was 8.75, the difference be- 
tween the means being significant at (t = 
2.67). 



DISCUSSION 

The molluscan shell is formed by the dep- 
osition of calcium carbonate on a protein ma- 
trix. For snails in a soft water environment, an 
immediate source of calcium could be ben- 
eficial to the developing juveniles and so 
there is an a priori reason for expecting snails 
to be able to detect and orientate towards 
calcium. The possible attractant properties of 
calcium were demonstrated here by the re- 
sults of Trial (i) on L. stagnalis. It appeared 
that sodium chloride did not act as a repel- 
lant, because movements away from this 
compound were not significant in Trial (ii); 
Madsen (1990) found that such snails as H. 
duryi and Bulinus truncatus Audouin were not 
adversely affected by low concentrations of 
sodium chloride. However, there could have 
been a significant aversion to the de-ionised 
water in Trial (ii). 

Young (1975) reported that in soft water, L. 
peregra extracted 70% of the calcium re- 
quirement from lettuce and in hard water, ex- 
tracted only 46% from lettuce. This was 
compared with L. stagnalis, which, although 
it efficiently extracted 95% of the calcium 
content of the lettuce, usually only took 20% 
of the total requirement from this source, the 
remaining 80% being derived directly from 
the water. Thus, the relationships between 
environmental base-ion concentration and 



11 



PIGGOTT & DUSSART 



TABLE 3. Results for eight L. peregra reared in hard water and eight reared in soft water. The snails 
were tested when they had reached an overall shell length of 6-8 mm. Calcium was presented as 100 
mg/l [Ca CI2.2H2O]. Each specimen was tested twice in each of the four orientations, i.e. 64 trials. 



Choice Available 



Result 



Snails reared in soft water 





[Ca^'l 


cf 


HgO^ 


Movements 


35 




14 


Snails reared in hard water 










[Ca^l 


cf 


НгО^ 


Movements 


22 




22 



Bias Towards.. x^ Significance 

[Ca^*] 8.2 P < 0.01 



neither 







N.S 



snail biology appear to be complicated. For 
example, ionic ratios might be involved; Har- 
rison et al. (1966) invoked the ratio of cal- 
cium/magnesium as a significant factor in 
egg production. There are also contrary re- 
sults; though Harrison et al. (1966) found a 
curvilinear relationship between egg produc- 
tion and calcium concentration for B¡- 
omphalaria pfelffeh, Thomas et al. (1974) 
found a positive linear relationship for Bi- 
omphalaha glabrata. Nevertheless, it ap- 
peared that in our experiments, the need to 
respond to a source of environmental cal- 
cium was less for L. peregra than for L. stag- 
nalis, possibly because L. peregra obtains a 
smaller proportion of its calcium require- 
ments direct from the environment. This 
proposition is supported by the results 
shown in Table 2; a gradually increasing re- 
sponse to a source of calcium by L. peregra, 
whereas the corresponding response of L. 
stagnalis was immediately highly significant. 
Even when kept, albeit temporarily, in hard 
water (84 mg/l [Ca^"^]), it seems that the cal- 
cium requirement of L. stagnalis was not be- 
ing met in these relatively small containers. 

Trials (v) to (xii) were designed to show 
species-specific differences in behaviour and 
were not particularly designed to distinguish 
between the effects of calcium, chloride or 
possible osmotic potential effects of de-ion- 
ised water. However, the results of trial (x) for 
L. peregra suggest that chloride and osmotic 
potential were not playing respectively at- 
tractive and aversive roles, because a major- 
ity of snails chose de-ionised water. There is 
also circumstantial evidence from Trials (i) to 
(iv) and from the literature to suggest that cal- 
cium is a significant factor (e.g., Greenaway, 
1971a, b). It is probable that ten L. stagnalis 
housed in one litre of pond water would re- 
duce the calcium concentration to such a 
level that a significant response to a source 
of calcium would be both essential for the 



snail and observable by the experimenter. 
For example, in our experiments, L. stagnalis 
showed a massive response to the source of 
calcium, having been in soft water for only 
one week. Out of 247 observed movements, 
186 were towards the source of calcium; if 
osmotic potential were the only factor, it 
might be expected that the response would 
not have changed between trials. In addition, 
at this stage, the shells of L. stagnalis were 
becoming increasingly fragile. Nduku & Har- 
rison (1976) suggested that snails cultured in 
low calcium concentration are physiologi- 
cally stressed and cannot carry out normal 
metabolic processes. 

Bielefeld et al. (1993) have implicated alka- 
line phosphatase in the mantle epithelium as 
a factor in shell mineralisation, and Green- 
away (1971a, b) suggested that there was a 
net movement of calcium from the environ- 
ment into the blood, excess calcium being 
deposited as carbonate in the shell. When 
Greenaway cultivated snails in soft water, 
there was a loss of calcium from the blood to 
the external environment. To compensate, a 
reverse flow of calcium occurred from the 
shell to the blood. It is therefore likely that in 
the later stages of our experiments, L. stag- 
nalis were physiologically stressed. 

Given that the test snails of both species 
were of similar sizes, these results suggest 
that either L. stagnalis has a greater calcium 
demand than L. peregra, or that L. peregra 
has a higher threshold for the inception of 
calcium-mediated stress at lower concentra- 
tions than L. stagnalis. The implication is 
therefore that in terms of meeting calcium re- 
quirements, the niche breadth of L. peregra is 
wider than that of L. stagnalis. This hypothe- 
sis is supported by Costil-Fleury (1991), who 
used factor analysis to show that L. peregra 
is less confined in terms of habit type than L. 
stagnalis. 

However, many other physico-chemical 



RESPONSE OF LYMNAEA TO ENVIRONMENTAL CALCIUM 



19 



and blotlc factors are as important as cal- 
cium. Temperature, pH, macro-vegetation, 
suspended solids and the nature of the 
allochthonous input to the habitat have all 
been suggested as crucial factors in mollus- 
can distribution (e.g., Macan, 1974; Okland, 
1983; Pip, 1986), and Dussart (1979) showed 
that potassium, mud substratum-type and 
rock substratum-type were major variables in 
the distribution of Bithynia tentaculata (L.), 
Gyraulus albus (Müller) and Planorbis planor- 
bis (L.) respectively; magnesium was a major 
water chemistry variable for L. peregra. 

The results of the investigation using L. 
peregra reared in different environmental 
conditions tentatively support the suggestion 
of Dussart (1979) that in soft waters, snails 
might satisfy a metabolic need for calcium by 
orientating towards, and laying eggs on 
shells. There is anecdotal evidence that, es- 
pecially in areas of base-ion deficiency, 
aquatic snails will aggregate on shells, bones 
and other calcium sources; it would be useful 
to compare the calcium responses of snails 
originating from soft-water environments 
with snails of the same species from hard- 
water environments. If raised in identical con- 
ditions, any significant differences in re- 
sponses persisting in the Fl and succeeding 
generations would indicate the existence of 
physiological races and plasticity. This in turn 
might suggest that the process of speciation 
for water type is under way. 

The existence of a microhabitat at the sub- 
stratum surface of, say, a shell or a pebble 
needs to be recognised. Environmental cal- 
cium concentration in the microhabitat could 
be higher at interfaces due to mineralization 
by bacteria, algae or fungi. Consequently, a 
variety of factors could act as a cue for ovi- 
position on shells, examples being biofilms 
(auchwuss) on the shell surface, phero- 
mones, amino acids from the shell protein, or 
even physical contact with the shell as a sub- 
stratum rather than the calcium itself. In the 
experiments reported here, it is possible that 
the differing physico-chemical nature of the 
plastic, pebble and shell surface had facili- 
tated the development of biofilms that might 
have differentially encouraged egg deposi- 
tion on these surfaces; this possibility needs 
further investigation. Conversely, if an amino- 
acid attractant was leaking from the shell sur- 
face, it could be species-specific, because 
the concentration of amino acids within 
shells differs in different species of mollusc 
and with waters of different hardness (Dus- 



sart, 1973; 1983). Freshwater snails can 
show chemoreception in relation to amino 
acids exuded from a food source (Croll, 
1983; Thomas et al., 1980), and the parent 
snails could be following an amino acid gra- 
dient to the target shell. In natural conditions, 
the amino acids could act as a primary stim- 
ulus and calcium could be secondary. The 
behavioural response to the amino acids in 
the shell of L. peregra could be examined by 
other choice-chamber experiments. How- 
ever, the possibility of synergism must be 
recognised; for example, Uhazy et al. (1978) 
noted a synergistic response of B. glabrata to 
the amino acids proline and glutamine. 

Despite the fact that Uhazy et al. (1978) 
found that ß. glabrata would orientate to- 
wards magnesium but not calcium, our dem- 
onstration of species-specific differences 
has implications for control of snail vectors of 
helminth disease; for example, species within 
the Bulinus and Biomphalaria genera might 
show similar variability. As suggested by 
Thomas et al. (1980), Thomas (1982) and 
Lombardo et al. (1991), baiting techniques 
might be used to control helminth vectors, 
and knowledge of the role of calcium could 
be an important contributing factor. 

In conclusion, it seems from this study that 
there are differences in orientation behaviour 
that might be symptomatic of the calciphile 
distribution of L. stagnalis compared with the 
eurycalcic distribution of L. peregra. In the 
investigation of oviposition-site behaviour of 
L. peregra, the bias towards laying eggs on 
shells may have been due to such factors as 
leakage of calcium or amino acids from the 
shells, or mechanical quality of the shell sur- 
face. Both species might be able to orientate 
towards sources of calcium, though aversion 
to a low osmotic potential and attraction to 
chlorides are alternative, though less likely 
hypotheses. Also, there appears to be a dif- 
ference in response within a species when 
the animals are raised under different envi- 
ronmental conditions, suggesting that there 
may be the capacity for physiological plas- 
ticity within these metabolic requirements. 



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RESPONSE OF LYMNAEA TO ENVIRONMENTAL CALCIUM 21 

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MALACOLOGIA, 1995, 37(1): 23-32 

ANATOMICAL STUDY ON TONNA GALEA (LINNÉ, 1758) AND 

TONNA MACULOSA (DILLWYN, 1817) (MESOGASTROPODA, TONNOIDEA, 

TONNIDAE) FROM BRAZILIAN REGION. 

Luiz Ricardo Lopes de Simone 

Seçào de Moluscos, Museu de Zoología da Universidade de Sao Paulo, 
Caíxa Postal 7172, CEP 01064-970, Sao Paulo, SP, Brazil 

ABSTRACT 

Tonna galea and Tonna maculosa, from Brazilian region, are described anatomically. Each 
character is compared between the species and also with other known Tonnoidea. These 
species differ anatomically in characters of the mantle color and collar, osphradium, hypobran- 
chial gland, kidney, proboscis length, radular rachidian, lateral tooth, penis, vas deferens, and 
female genital opening. Characters of the anterior region of the digestive system, heart, penis 
and palliai oviduct are of particular interest in tonnoidean systematics. 



INTRODUCTION 

Tonna galea (Linné, 1758) is a very v\/ide- 
ranging species, occurring in the Pacific and 
Atlantic oceans and in the Mediterranean 
Sea. Tonna maculosa (Dillv\/yn, 1817), in con- 
trast, only occurs in the tropical west Atlantic 
(Ríos, 1985: 70; Matthews et al., 1987: 33). 
Tonna perdix (Linné, 1 758), which is closely 
related to T maculosa, occurs in the Indo- 
Pacific region, and some authors consider 
them to be synonyms (e.g., Morretes, 1949). 
Two questions arise: (1) is "Tonna galea" a 
single species, and (2) are T maculosa and T 
perdix really separate species? These ques- 
tions have been discussed (e.g., Turner, 
1948; Matthews et al., 1987), with arguments 
based on shell characters, but are still unre- 
solved. 

The objective of this paper is not to answer 
these questions, but to be a step in this di- 
rection, providing anatomical descriptions of 
specimens identified as Tonna galea and T 
maculosa from the Brazilian region. These 
data could be used in comparisons with sup- 
posed co-specific specimens from other ar- 
eas to assist in clarifying the systematic 
problems. Another objective of this paper is 
to contribute to the understanding of system- 
atic characters in the Tonoidea, identifying 
some useful characters not previously uti- 
lized in the systematics of this group. 

Little has been published on the anatomy 
of the Tonnoidea, and in particular the Ton- 
nidae. What has been has mainly concerned 
the alimentary canal and feeding habits. The 



following information is available: Tonna 
galea: Weber (1927) studied the digestive 
system, and some of his data were repro- 
duced by Hyman (1967); Turner (1948) 
described the penis and figured the radula; 
Matthews et al. (1987) figured the penis, 
jaw and radular rachidian; and Bentivegna & 
Toscane (1991: 37) figured an active speci- 
men preying on Holothuria tubulosa and 
H. sanctori. Tonna maculosa: Turner (1948) 
described the penis and figured the radula; 
and Matthews et al. (1978) figured jaw 
and radular rachidian. Other Tonnoidea de- 
scribed anatomically and used here for com- 
pahsion are: Reynell (1905)— description of a 
male Cassidaria rugosa (Linné) (Ranellidae); 
Day (1969) — digestive system of Argobuc- 
cinum argus (Gmelin) (Ranellidae); Houbrick 
& Fretter (1969) — digestive system and 
other organs of three species of Bursa (Bur- 
sidae) and four of Cymatium (Ranellidae); 
Lewis (1972) — anatomy of anterior region of 
digestive system, head-foot complex and pe- 
nis of Distorsio perdistorta Fulton (Ranell- 
idae); and Hughes & Hughes (1981) — diges- 
tive system of Cassis tuberosa (Linné), 
(Cassidae). 

MATERIAL AND METHODS 

The specimens studied belong to malaco- 
logical collection of the Museu de Zoología, 
Universidade de Sao Paulo (MZUSP). They 
are preserved in 70% ethanol. 

All specimens were dissected using stan- 
dard techniques. The buccal region, region of 



23 



24 



SIMONE 



female genital opening and palliai oviduct 
were extracted, dehydrated in ethanol series, 
stained by carmine, cleared, and fixed with 
creosote. Radulae and jaws were examined 
on slides with Hoyer. All drawings were made 
using a camera lucida. 

Anatomical terminology is based on Rey- 
nell (1905) and Hughes & Hughes (1981). 
Conchological description and synonymy are 
omitted, and can be found mainly in Mat- 
thews et al. (1987) and Turner (1948). 

Tonna galea (Linné, 1758) 
(Figs. 1-19, 37) 

Synonymy and types material: Turner 
(1948: 173) and Matthews et al. (1987: 31) 

Diagnosis 

Shell of clear, homogeneous color; outline 
globose; sculptured with strong, spiral, 
somewhat isomethcal ridges. Mantle border 
thick; hypobranchial gland poorly developed. 
Kidney large, with complex tissue arrange- 
ment. Proboscis about half projecting from 
rhynchodeum in fixed specimens. Central 
cusp of radular rachidian smooth; main cusp 
of lateral tooth smooth. Penis with a small 
pointed papilla; anterior region of vas defer- 
ens fused with seminal receptaculum. Fe- 
male genital opening with larger inner divi- 
sion for the bursa opening. 

Description 

Shell: Detailed descriptions of the shell given 
by Turner (1948: 173 pi. 78) and Matthews et 
al. (1987: 31, figs. 1,2). Protoconch brown, of 
almost four glassy, convex whorls. 

Head-Foot Complex (Figs. 1 , 2): Foot large, 
solid, rounded posteriorly, notched anteri- 
orly; propodium narrow, with anterior pedal 
gland opening to ventral slit (Fig. 1, mp). 
Operculum lacking in adult, present in young 
(Rios, 1985). Tentacles long, fairly thick, 
bluntly pointed. Black eyes on tubercles on 
outer upper part of tentacle bases. Rhyncho- 
deum with simple, rounded opening. Probos- 
cis with about half of length projecting from 
rhynchodeum in all specimens (Fig. 2). Head- 
foot structures beige, with dark brown, irreg- 
ular spots. 

Palliai Complex (Fig. 12): Mantle edge entire, 
simple, not reflected, thick, rounded, pale 
cream in color. Palliai cavity occuping first 



whorl. Siphon long, well developed, pale- 
beige, with dark-brown, somewhat longitudi- 
nal, irregular spots. Osphradium large, bipec- 
tinate, on palliai roof at base of siphon; 
osphradium leaflets lamellate, pigmented 
brown. Ctenidium very large, monopectinate 
(Fig. 12); leaflets very numerous, triangular, 
low. Hypobranchial gland not well devel- 
oped; some specimens with folds of this 
gland running from the anterior and left re- 
gion of rectum. Flaccid tissue covering rec- 
tum (and palliai oviduct in females) on right 
side of mantle cavity, allowing a well-devel- 
oped ad-rectal sinus. 

Excretory-Circulatory Systems: Kidney very- 
large, on right side of pericardium, immedi- 
ately behind palliai cavity, from which it Is 
separated by a thin, nearly transparent mem- 
brane (Fig. 12, km); this membrane with slit- 
like nephrostome, surrounded by muscular 
fibres to form a sphincter (Fig. 12, ne). Kidney 
traversed by intestine, which divides it into 
two lobes, the largest (Fig. 13) anterior, the 
smallest posterior. Internally, the kidney is 
very complex, the outer divisions being 
formed by green-brown lobes and tubes, its 
anterior limit bulging the posterior region of 
palliai oviduct glands of females. Nephridial 
gland cream-colored, poorly developed, sit- 
uated above nephrostome (Fig. 13, ng). Heart 
(Fig. 13) with very thin, transparent, flaccid 
auricle and a very thick, rounded ventricle 
(Fig. 13). Ctenidial vein on right margin of gill, 
entering auricle both anteriorly and posteri- 
orly (Fig. 13). Central part of auricle inserting 
directly in gill margin (Fig. 13, au). 

Ad-rectal sinus very developed, apparently 
continuous from chamber of kidney into an 
aperture, with muscular walls, near the anus 
(Fig. 37, at), similar to an ureter. 

Digestive System: Similar to that described 
by Weber (1927), typical of tonnoideans 
(Hughes & Hughes, 1981). Some details of 
insertion of proboscis gland duct and oe- 
sophagial caecum duct in buccal complex 
are shown in Figure 4; detail of buccal com- 
plex (sectioned dorsally) shown in Figure 5; 
transversal section of the mid region of ante- 
rior oesophagus shown in Figure 6. Salivary 
glands surrounding duct of proboscis gland 
(Fig. 3). Duct of each proboscis gland looping 
anteriorly to nerve ring in all specimens ex- 
amined (Fig. 1 1). Radular rachidian tricuspate 
(Fig. 7; Matthews et al., 1987); lateral teeth 
with a flattened, irregular base and two 
cusps, a long, large acuminate cusp and a 



ANATOMICAL STUDY ON TONNA GALEA 



25 




FIGS. 1-1 1 : Tonna galea: (1) head-foot complex from a male, scale = 10 mm; (2) the same, with proboscis 
sheath exposed, scale = 10 mm; (3) anterior region of digestive system, dorsal view, scale = 10 mm; (4) 
anterior extremity of opened proboscis, right-dorsal view, scale = 1 mm; (5) buccal complex opened 
dorsally, inner view, scale = 2 mm; (6) transversal section in mid region of the anterior oesophagus, ventral 
region down, scale = 1 mm; (7) rachidian tooth of the radula; (8) lateral tooth showing the accessory cusp 
(ac); (9) inner marginal tooth; (10) outer marginal tooth, scale (Figs. 7-10) = 0.5 mm; (11) dorsal view of the 
region of nerve ring, scale = 2 mm. 



26 



SIMONE 




FIGS. 12-19: Tonna galea: (12) inner view of palliai cavity and viceral mass of a male, scale = 10 mm; (13) 
detail of opened nephridial and pericardial chambers, scale = 2 mm; (14) viceral mass of a male, mantle 
partially removed, scale = 2 mm; (15) ventral view of the penis, scale = 2 mm; (16) detail of insertion region 
of the vas deferens in seminal groove, showing the receptaculum, scale = 2 mm; (17) palliai oviduct, 
tegument removed, scale = 10 mm; (18) detail of the albumen gland showing the vesicles (ve). scale = 2 
mm; (19) detail of female genital pore, tegument removed, scale = 2 mm. 



ANATOMICAL STUDY ON TONNA GALEA 



27 



minute cusp (Fig. 8, ac); base of inner mar- 
ginal teeth (Fig. 9) a little longer than that of 
outer marginal teeth (Fig. 10). Stomach 
poorly developed, with two ducts to digestive 
glands, without developed style sac, folds or 
typhlosole. 

Nervous System: Nerve ring (Fig. 11 , nr) with 
cerebral ganglia turned to left side in all spec- 
imens; from these, three pairs of nerves run 
anteriorly, fusing near the proboscis gland 
duct loops to become only one pair, which lie 
ventraly to the oesophagus (Fig. 11, np). In 
mid oesophagial region, this pair of nerves 
bifurcates, the median nerves (Fig. 6, in) in- 
nervating radular bulb and the lateral nerves 
(Fig. 6, on) innervating proboscis wall. 

Genital System, Male: Testis (Fig. 14, tt) 
branching into digestive gland, mainly on col- 
umellar surface of viceral mass. Convoluted 
seminal vesicle rather spheric (Fig 14, pt), 
confined to anterior part of viceral mass just 
anterior to testis. Vas deferens thin walled 
(Fig. 14), its anterior region to right of the re- 
ceptaculum, fused with its walls (Fig. 16). Re- 
ceptaculum a modified, bulging region of the 
spermatic groove posterior to vas deferens 
insertion in spermatic groove (Fig. 16). In 
floor of right margin of palliai cavity, sper- 
matic groove thick walled near prostate 
gland (Figs. 1,14,16). Penis large, somewhat 
flattened, with open penial groove, which ter- 
minates in a small, pointed papilla at central 
region of penis tip (Fig. 15). 

Female: Ovary branching into digestive 
gland. Oviduct slender (Fig. 17), with a small 
gonopehcardial duct. Oviduct opening into a 
short, thick-walled albumen gland. A series 
of small, paired vesicles present in ventral 
side of the albumen gland (Figs. 17, 18, ve). 
Capsule gland long, curved, thick walled (Fig. 
17). Bursa copulatrix long, claviform, sepa- 
rate and to right of capsule gland. Posterior 
limit of bursa sacciform, thin walled, the walls 
gradually becoming thickly muscular anteri- 
orly (Figs. 17, 19, be). Genital pore small 
(Figs. 17, 19, gp), to right, behind anus; pore 
with two inner divisions: the largest and pos- 
terior is the end of the bursa, the smallest and 
anterior the end of palliai oviduct (Fig. 19). 

Measurements 

Length, width in mm and if mature (m) or 
immature (i): MZUSP 27967: male, 78.5 by 
66.5, m; female, 73.0 by 61.0, i; male, 69.5 



by 55.5, m; MZUSP 27984: male, 74.2 by 
60.6, m; MZUSP 27968: female, 102.0 by 
85.0, m; MZUSP 27986: male 1 1 8.5 by 1 04.0, 
m: MZUSP 27969: female 1 35.0 by 1 1 5.0, m; 
male 98.7 by 71.0, m. 

Habitat 

The specimens were obtained by diving, 
burrowing in sandy sediment, near rocks or 
reefs. Some specimens were also dredged 
from about 150 m depth in muddy sediment. 

Material Examined 

BRAZIL. Espirito Santo: MZUSP 27970, 1 
male and 1 female. Barra do Riacho (8/ix/72). 
Sao Paulo: MZUSP 27967, 2 males and 1 
female, Saco da Ribeira Beach, Ubatuba 
MZUSP 27983, 2 females, Enseada Beach 
Ubatuba (x/91); MZUSP 27984, 1 male, est. 
42, otter traw (22/x/86); MZUSP 27985, 1 
male, lOUSP-Veliger, "rede de pesca fixa 8" 
URUGUAY, off Maldonado: MZUSP 27968, 1 
female, 35'^18'S 52°32'W, "W. Besnard,' 
station 1920, 150 m deep (30/x/72); MZUSP 
27969, 2 males and 1 female, same data 
MZUSP 27986, 4 males and 1 female, "W. 
Besnard," station 1921 0T.9 (20/x/72). 

Tonna maculosa (Dillwyn, 1817) 
(Figs 20-36) 

Synomymy and type material: Turner 
(1948: 169) and Matthews et al (1987: 37) 

Diagnosis 

Shell dark-brown, spotted; outline fusi- 
form; sculpture of low spiral ridges. Mantle 
border thin. Hypobranchial gland developed. 
Kidney with a smooth surface. Proboscis to- 
tally within rhynchodeal cavity in fixed spec- 
imens. Radular rachidian with crenulations 
on base of central cusp; crenulation on main 
cusp of lateral radular teeth. Penis without 
papilla, with a flap of the tegument on tip. 
Anterior region of vas deferens separated 
from walls of receptaculum. Inner division in 
female genital opening of capsule gland 
larger than in T galea. 

Description 

Shell: Detailed decriptions of shell are given 
by Turner (1 948: 1 69-1 72, pi. 75, fig. 2, pi. 76, 
figs. 1, 2) and Matthews et al. (1987: 37, fig. 



28 



SIMONE 



6). Protoconch of almost four glassy, convex 
whorls, brown In color (Figs. 20, 21). 

Head-Foot Complex (Fig. 22): Foot solid, 
large, rounded posteriorly, notched anteri- 
orly; propodium narrow, with anterior pedal 
opening to ventral slit (Fig. 22, mp). Opercu- 
lum lacking in adult. Tentacles long, fairly 
thick, bluntly pointed (Fig. 22). Black eyes on 
tubercles on outer upper part of tentacle 
base. Rhynchodeum with simple, rounded 
opening. Proboscis completely retracted 
within proboscis sheath in all specimens. 
Color of all head-foot structures beige, with 
clear-brown irregular spots. 

Palliai Complex (Fig. 31): Mantle edge entire, 
simple, not reflected, thin, flattened, pale 
cream in color. Palliai cavity occupying first 
whorl. Siphon long, well developed, pale- 
beige in color, with clear-brown irregular 
spots. Osphradium large, bipectinate, pro- 
portionaly larger than that of T. galea, situ- 
ated on palliai roof at base of siphon; osphra- 
dium leaflets lamellate, pigmented brown. 
Ctenidium very large, monopectinate, with 
many low, triangular filaments. Hypobran- 
chial gland developed, along left side of an- 
terior region of rectum. Tissue covering rec- 
tum and palliai oviduct of females less flaccid 
than that of T. galea, but allowing a well-de- 
veloped ad-rectal sinus. 

Excretory-Circulatory Systems: Kidney mod- 
erately large (Fig. 30), forming a sac situated 
like that of T. galea. Well-developed, slit-like 
nephrostome, surrounded by muscular fibres 
to form a sphincter (Figs. 30, 31 , ne). Internal 
structures of kidney similar, but simpler than 
in T. galea, with a smooth surface and a 
cream color; its anterior limit does not bulge 
with albumen gland of females. Nephridial 
gland somewhat inconspicuous, situated 
dorsal to nephostome (Fig. 30, ne). Heart 
(Figs. 30, 31) with a very thin, transparent, 
flaccid walled auricle, and a very thick-walled, 
rounded ventricle. Ctenidial vein and auricle 
like those of T. galea. 

Ad-rectal sinus well developed but less 
than that of T. galea; as in that species, sinus 
apparently continuous from kidney chamber 
into an aperture (Figs 35, 36, at), with mus- 
cular walls, near anus, like an ureter. 

Digestive System: Like that of T. galea (Figs. 
23-29). Structures within buccal bulb very 
similar to those of T. galea; a pair of ventral 
jaws (Fig. 24, md), two dorso-lateral folds (If) 
in buccal cavity, one on either side, with 



opening of proboscis gland duct median to 
fold and near its anterior end. Radula with 
rachidian with a crenulation on base of its 
central cusp; tip of this cusp slender and 
smooth (Fig. 26). Lateral teeth with a series of 
crenulations on main cusp (Fig. 25, cr); small 
accessory cusp present (Figs. 25, 27, ac). In- 
ner (Fig. 28) and outer (Fig. 29) marginal teeth 
similar of those of T. galea. Oesophagus and 
its inner ventral folds and glands similar to T. 
galea, but much shorter (Figs. 23, 24). Oe- 
sophageal caecum present, the folds and 
glands of the oesophagus terminating in os- 
tium of caecum (Fig. 24, eo). Posterior oe- 
sophagus without distinct glands or crop. 
Stomach poorly developed, with two ducts to 
digestive glands, but without developed style 
sac, folds, or typhlosole. Inner surface of 
posterior oesophagus, stomach and intestine 
with low longitudinal folds. Salivary glands, 
proboscis glands and their ducts (Figs. 23, 
24), similar of those of T. galea (Weber, 1 927). 
All anterior structures of digestive system 
maintained in position by a tridimensional net 
of muscle fibres running to wall of oesopha- 
gus, body wall and foot. Looping section of 
ducts of proboscis gland lying anterior to 
nerve ring, as in T. galea. 

Nervous System: Nerve ring (Fig. 23, nr) with 
cerebral ganglia turned to left side in all spec- 
imens examined. Ventral pair of nerves of 
proboscis similar to those of T. galea. 

Genital System, Male: Testis branching into 
digestive gland, concentrated mainly on col- 
umellar surface of viceral mass. End of vas 
deferens an enclosed, small, thin-walled 
tube, lying to right of receptaculum, without 
fusion except for insertion (Fig. 34). Recep- 
taculum a modified, bulging region of sper- 
matic groove, posterior of insertion of vas 
deferens in floor of palliai cavity (Fig. 34). 
Spermatic groove in right side of floor of pal- 
liai cavity, thick walled, by the prostate gland 
(Figs. 22, 32, 33, 34). Penis very large (Figs. 
32, 33), curved backwards, somewhat flat- 
tened, its free end curving downwards fol- 
lowing curve of floor of palliai cavity, blunt at 
the apex. At right side, near apex of penis 
there is a flap of tissue (fig. 32: pf), under 
which the penial duct opens; there is no pa- 
pilla. 

Female: Ovary branching into digestive 
gland. Oviduct slender, opening into a short, 
thick-walled albumen gland (Fig. 35). A series 
of paired vesicles present in ventral side of 



ANATOMICAL STUDY ON TONNA GALEA 
2} 



29 




FIGS. 20-31; Tonna maculosa: (20) protoconch in profile; (21) protoconch, apical view, scale (Figs. 20, 21) 
= 2 mm; (22) head-foot complex from male, scale = 5 mm; (23) dorsal view of anterior region of the digestive 
system, proboscis opened, scale = 5 mm; (24) the same, oesophagus opened longitudinally, scale = 5 mm; 
(25) lateral tooth of radula, showing the crenutation (cr) and the accessory cusp (ac), scale = 0.1 mm; (26) 
rachidian tooth; (27) lateral tooth; (28) inner marginal tooth; (29) outer marginal tooth, scale (Figs. 26-29) = 
0.2 mm; (30) detail of opened nephidial and pericardial champers, scale = 2 mm; (31) palliai cavity of a male, 
inner view, scale = 5 mm. 



30 



SIMONE 




FIGS. 32-36: Tonna maculosa: (32) penis and seminal groove, dorsal view: (33) the same, ventral view, 
scale = 5 mm; (34) detail of the insertion of vas deferens in seminal groove, showing the receptaculum, 
scale = 1 mm; (35) palliai oviduct ventral view, tegument partially removed, scale = 5 mm; (36) detail of 
female genital pore, tegument removed, scale = 2 mm. 



albumen gland, similar to those of T. galea, 
Capsule gland long, curved, thick walled (Fig. 
35, eg). Bursa copulatrix long, claviform, 
slender, separate and to right of capsule 
gland; posterior end of the bursa sacciform, 
thin walled, the walls becoming thick and 
muscular anteriorly (Fig. 35, be). Small genital 
opening at right and posterior to anus (Figs. 
35, 36, gp). Genital opening with two inner 
divisions, the smallest and posterior is end of 
bursa (be), and the larger and anterior is end 
of capsule gland (eg) (fig. 36). 

Measurements 

MZUSP 27961, female = length 65.0 mm 
by width 44.0 mm; male = 40.4 mm by 26.5 
mm. MZUSP 27962, female = 45.3 mm by 
31.0 mm. 

Habitat 

The collected specimens were found by 
diving or at low tide, burrowing on sandy bot- 
toms near reefs. 



Material Examined 

BRAZIL. Bahia: MZUSP 27961 (one male 
and one female) Itapuä Beach, Salvador (7/ 
vii/71); MZUSP 27962 (one female) Itapuä, 
Salvador (29/ix/84). 



DISCUSSION 

Tonna galea differs anatomically from T. 
maculosa in having (1) a thick mantle border; 
(2) darker spots on the epidermis; (3) a less- 
developed hypobranchial gland; (4) a propor- 
tionally smaller osphradium; (5) a more de- 
veloped kidney, with more complex internal 
structure; (6) proboscis extending 50% from 
rhynchodeum (in T. maculosa proboscis al- 
ways completely retracted within proboscis 
sheath) in fixed specimens; (7) oesophagus 
and inner oesophagial structures much 
longer; (8) central cusp of radular rachidian 
teeth and lateral teeth without crenulations 
(present in T. maculosa); (9) penis with a pa- 



ANATOMICAL STUDY ON TONNA GALEA 



31 




FIG. 37: detail of anal region of Tonna galea, scale 
= 2 mm. 



pilla (T. maculosa has a flap, without papilla); 
(1 0) end region of vas deferens fused with the 
receptaculum walls (in T maculosa this duct 
is free); and (11) female genital pore with 
larger inner opening to the bursa (Г. macu- 
losa has the larger opening leading to the 
capsule gland). 

The function of the aperture near the anus 
(Figs 36, 37, at) in both species is unknown. It 
probably controls the exit of the inner fluid of 
the ad-rectal sinus, which is apparently con- 
tinuous to the kidney chamber. These struc- 
tures resemble the ureter of the Viviparidae 
(Hyman, 1967), for example, which have no 
well-developed nephrostome as in Tonna 
(Figs. 21, 31, ne). The fortuitous use of the 
ad-rectal sinus as an ureter merits further 
study. 

Some differences between the literature 
accounts (Turner, 1948; Mattews et al., 1987) 
and the specimens studied here were: (1) the 
protoconchs of both species are closely sim- 
ilar, and of almost four whorls, in contrast 
with the data of Matthews et al. (1987), in 
which differences in number of whorls was 
given; (2) the jaw lies ventral to the proboscis; 
(3) the radular rachidian of T. maculosa has a 
crenulation only on the base of the central 
cusp; the tip of this cusp is smooth and slen- 
der (Fig. 26, or); (4) the radular lateral tooth 



has a small, but conspicuous accessory 
basal cusp in all specimens examined of both 
species (Figs 8, 25, 27, ac); (5) Turner (1948: 
168) reported an extremely long and flagel- 
late papilla in the penis of T. maculosa, dif- 
ferent from the penis described herein, in 
which the papilla is lacking (Figs. 32, 33). Fur- 
ther investigation is need to determine the 
significance of these differences. 

The proboscis of Tonna, as in all known 
Tonnoidea, has a great development of the 
buccal mass, this region taking most of the 
proboscis length (Figs. 2, 23). The proposal 
of the tonoidean proboscis as a distinct type 
(Day, 1969) is perhaps not justified, but rather 
it can be regarded as a specialized and mod- 
ified pleurembolic type. 

The auricle structure and palliai oviduct 
may be considered as additional characters of 
Tonnoidea, in addition to the anterior region of 
the digestive system. This type of auricle is 
found in Cassidaha rugosa (Ranellidae) (Rey- 
nell, 1905). However, no reference to the pal- 
liai oviduct has been found in the literature 
except for Bursa cruentata (Houbrick & Fret- 
ter, 1969: 417), but details are missing that 
would allow a full comparison. 

Besides radular aspects, other charac- 
ters of the Tonna digestive system differing 
from other Tonnoidea (Reynell, 1902; Day, 
1969; Houbrick & Fretter, 1969; Lewis, 1972; 
Hughes & Hughes, 1981) are (1) the presence 
of a oesophagial caecum and (2) the absence 
of a clear oesophagial gland (crop or bulb) in 
the posterior oesophagus. These are per- 
haps characters of Tonnidae. 



LITERATURE CITED 

BENTIVEGNA, F. & A. TOSCANO, 1991, Observa- 
tion au laboratoire sur le comportement alimen- 
taire de trois espèces de la superfamille Ton- 
noidea (Mollusca, Gastropoda). Revue Française 
d'Aquariologie Herpetologie, 18: 33-38 

DAY, J. A., 1969, Feeding of the cymatiid gastro- 
pod, Argobuccinum argus, in relation to the 
structure of the proboscis and secretions of the 
proboscis gland. American Zoologist, 9: 909- 
916 

HOUBRICK, J. R. & V. FRETTER, 1969, Some as- 
pects of the functional anatomy and biology of 
Cymatium and Bursa. Proceedings of the Mala- 
cological Society of London, 38: 415-429 

HUGHES, R. N. & H. P. I. HUGHES, 1981, Mor- 
phological and behavioural aspects of feeding in 
the Cassidae (Tonnacea, Mesogastropoda). Ma- 
lacologia, 20: 385-402 



32 



SIMONE 



HYMAN, L. H., 1967, The invertebrates, Volume VI, 
Mollusca I. McGraw-Hill Book Company. New 
York, 792 pp. 

LEWIS, H. 1972, Notes in the genus Distorsio (Cy- 
matiidae) with descriptions of new species. Nau- 
tilus, 86: 27-50 

MATTHEWS, H. R.; J. H. N. LEAL & A. С S. CO- 
ELHO, 1987, Superfamilia Tonnacea no Brasil. 
VII — Familia Tonnidae (Mollusca: Gastropoda). 
Arquivos de Ciencias do Mar, 26: 29-45 

MORRETES, F. L., 1949, Ensaio de catálogo dos 
moluscos do Brasil. Arquivos do Museu Para- 
naense, 7: 2-216 

REYNELL, A., 1905, Some account of the anatomy 
of Cassidaria rugosa (Linn.). Proceedings of the 
Malacological Society of London, 6: 292-299, pi. 
6 

RIOS, E. C, 1985, Sea sliells of Brazil. Fundaçâo 
Universidade de Rio Grande, Fundaçâo Cidade 
de Rio Grande, Museu Oceanógrafico. Rio 
Grande 239 pp., 102 pis. 

TURNER, R. D., 1948, The family Tonnidae in the 
western Atlantic. Johnsonia, 2: 165-192 

WEBER, H., 1927, Der Darm von Dolium galea L. 
eine vergleichend anatomische Undersuchung 
unter besonderer Berücksichtigung der Trito- 
nium Arten. Zeitschirift für Morptiologie und 
Ökologie der Tiere, 8: 663-804 



Revised Ms. accepted 26 October 1994 



ABBREVIATIONS 



ас: 


accessory cusp of lateral tooth 


ag: 


albumen gland 


ао: 


anterior aorta 


an: 


anus 


at: 


aperture of ad-rectal sinus 


au: 


auricle 


be: 


bursa copulatrix 


bu: 


buccal complex 


cf: 


central fold of buccal complex 


cm: 


columellar muscle 


cp: 


capsule gland 


cr: 


crenulated ridge 


cv: 


ctenidial vein 


dc: 


duct of oesophagial caecum 


dg: 


digestive gland 


dp: 


duct of proboscis gland 


ec: 


oesophagial caecum 


eo: 


ostium of oesophagial caecum 



fp: floor of palliai cavity 

ft: foot 

gc: gonopericardial duct 

gi: gill 

gp: female genital opening 

hg: hypobanchial gland 

in: inner proboscis nerve 

it: intestine 

ki: kidney 

km: membrane between kidney and 

palliai cavities 

If: lateral fold of buccal complex 

li: buccal lips 

mb: mantle border 

md: mandibule (jaw) 

mf: muscle fibers 

mg: mid-ventral mucous gland of 

oesophagus 

mo: mouth 

mp: anterior pedal gland 

ne: nephrostome 

ng: nephhdial gland 

nr: nerve ring 

oe: anterior oesophagus 

of: oesophagial folds 

on: outer proboscis nerve 

op: posterior oesophagus 

os: osphradium 

ov: oviduct 

pa: posterior aorta 

pb: proboscis 

pc: pericardial chamber 

pe: penis 

pf: penian flap 

pg: penian seminal groove 

pn: proboscis nerve 

po: proboscis gland 

pp: penian papilla 
pr -I- pt: convoluted seminal vesicle 

ra: radular complex 

re: proboscis sheath 

re: receptaculum seminalis 

rn: radular nucleus 

rs: rhynchodeum 

rt: rectum 

sa: salivary gland 

sg: seminal groove 

si: siphon 

te: cephalic tentacle 

tt: testis 

vd: vas deferens 

ve: vesicles of albumen gland 

vt: ventricle 



MALACOLOGIA, 1995, 37(1): 33-40 



A TAXONOMIC APPLICATION OF MULTIVARIATE MIXTURE 
ANALYSIS IN PATELLIDAE 

J. D. Acuña^ & M. A. Muñoz^ 



ABSTRACT 

Multivariate mixture analysis is a powerful tool that appears to be useful for dealing with 
situations in which several traits with overlapping variation are used for species discrimination. 
A multivariate mixture analysis technique is applied to discrimination of two sibling species of 
the genus Patella (P. áspera Röding and P. caerulea Linnaeus). These species show a sub- 
stantial overlap in the distribution of maximum shell width and shell height. In spite of this 
overlap, the results of mixture analysis in a sample of 101 specimens, classified but treated as 
unclassified for the purpose of the analysis, suggest the existence of two mixed distributions. 
Moreover, examination of specimen classification derived from mixture analysis reveals that 
these mixed distributions correspond to P. áspera and P. caerulea. The estimated values of 
mixture parameters confirm a substantial overlap in the bivariate distribution of maximum shell 
width and shell height of the two species. We hope that these results will contribute to making 
multivariate mixture analysis more popular among taxonomists. 

Key words: multivariate mixture analysis, taxonomy, species discrimination, Gastropoda, 
Patellidae, Patella áspera, Patella caerulea. 



INTRODUCTION 

Individual variation in morphological traits 
often provides valuable information for spe- 
cies discrimination. However, the interpreta- 
tion of variation is sometimes difficult due to 
polymorphism, polytypy, and similarity be- 
tween species. 

A particularly difficult case arises when 
species overlap in the distribution of contin- 
uous morphologic traits used for their classi- 
fication. Overlap in these traits can be mis- 
takenly interpreted as evidence in favor of 
interbreeding when, in fact, two or more non- 
hybridizing species are involved. 

The solution to this problem requires a de- 
tailed analysis of trait variation which is fre- 
quently made resorting to several statistical 
methods. However, taxonomists have not 
taken full advantage of recent advances in 
statistics to deal with the problem of overlap- 
ping variation. Mixture analysis techniques 
offer a useful alternative to traditional meth- 
ods of statistical analysis when overlapping 
variation is a concern (Everitt & Hand, 1981; 
Titterington et al., 1985; McLachlan & Bas- 
ford, 1988). 

Although originally developed to deal with 
problems in the biological realm (Pearson, 



1894), mixture analysis has received little at- 
tention from biologists. This may be in part 
due to difficulties in the computations re- 
quired by the method. Recently, several au- 
thors have confirmed the usefulness of mix- 
ture analysis for species discrimination (Do & 
McLachlan, 1984), the resolution of the age- 
class structure of a population (Equihua, 
1988), and the study of sexual dimorphism 
(Flury et al., 1992). 

In a previous report (Muñoz & Acuña, 
1994), we were able to discriminate between 
two sibling species of the genus Patella (P. 
áspera Röding and P. caerulea Linnaeus) by 
means of a univariate mixture analysis tech- 
nique. The specimens included in the sample 
were actually classified, but for the purpose 
of the analysis they were treated as unclas- 
sified. The taxonomic trait that we selected 
was shell height. Our aim was to show the 
usefulness of mixture analysis as a tool for 
species discrimination using a trait with over- 
lapping variation. Here we attempt the dis- 
crimination of these two species with the 
same method but using two conchological 
traits, which requires the use of multivariate 
mixture analysis. Multivariate mixture analy- 
sis provides powerful techniques for dealing 
with situations in which several traits with 



''Departamento de Biología Animal, Universidad de Valencia, Dr. Moliner, 50, 46100 Burjasot, Valencia, España. 
^Departamento de Ciencias Morfológicas I, Universidad Complutense de Madrid, Arcos de Jalón, s/n, 28037 Madrid, 
España. 



33 



34 



ACUNA & MUÑOZ 



overlapping variation are used for species 
discrimination. We hope that our results will 
contribute to making multivariate mixture 
analysis more popular among taxonomists. 



PATELLA ÁSPERA AND 
PATELLA CAERULEA 

Patella áspera Röding (= P. ulyssiponensis 
Gmelin) and P. caerulea Linnaeus are two 
very abundant European marine gastropods. 
The first is found in the Mediterranean and is 
also widely distributed along the Atlantic 
coast, whereas the second is restricted to the 
Mediterranean. The two species live in very 
similar habitats. Both are found on hard sub- 
strata in the littoral zone and reach upper 
subtidal levels, although P. áspera has a 
lower distribution range in the littoral zone 
and exhibits a preference for areas exposed 
to wave action. From a taxonomic stand- 
point, P. áspera and P. caerulea are consid- 
ered two separate species, although their 
specific status was a contentious issue for 
some time. 

Part of the protracted debate regarding the 
taxonomic status of these two species came 
about because there is substantial overlap in 
the distribution of traits (shell shape, orna- 
mentation, and coloration) used for their clas- 
sification. In the past, taxonomists interpreted 
this overlap as arising from interbreeding and 
accordingly rejected a specific distinction or 
considered this to be an instance of incom- 
plete speciation (Fischer-Piette, 1935, 1938; 
Evans, 1953, 1958). Others, however, argued 
that reproductive features (e.g., timing of the 
breeding season) could be used as a basis for 
discriminating between the two species (Fi- 
scher-Piette, 1948). The controversy was fi- 
nally settled when Fischer-Piette & Gaillard 
(1959) reported clear-cut species differences 
in the single cusp lateral teeth of the radula. 
More recently, analyses of a variety of taxo- 
nomic traits has confirmed the taxonomic va- 
lidity of Patella áspera and P. caerulea. Such 
is the case of studies that relied on caryotypic 
(Cervella et al., 1 988), electrophoretic (Sella et 
al., 1989; Cretella et al., 1990) and soft-part 
traits (Cretella et al., 1990). 

A review of the literature reveals that con- 
chological traits, when taken altogether, allow 
for a separation of the two species. Indeed, 
several authors have relied on conchological 
traits to separate samples, the species mem- 
bership of which was later confirmed by dif- 



ferences in radular (Fischer-Piette & Gaillard, 
1 959), electrophoretic (Cretella et al., 1 990), or 
soft-part traits (Cretella et al., 1990). Never- 
theless, taxonomists were reluctant to grant 
these Patella their current specific status until 
clear-cut differences were found in non-con- 
chological traits. This may be partly due to the 
difficulties involved in analyzing shell traits 
with overlapping variation. 



MATERIALS AND METHODS 

Our study of shell height by means of 
univariate mixture analysis (Muñoz & Acuña, 
1994) used a very large sample. Part of this 
material was judged suitable for the present 
study. 

The complete sample (detailed description 
in Muñoz & Acuña, 1994) included over a 
thousand specimens of Patella áspera and P. 
caerulea obtained at Cabo Oropesa, Castel- 
lón, España. Specimens of all available sizes 
were collected randomly in a narrow band of 
uniform characteristics located at the base of 
the littoral zone. Sampling took place in May 
1989. In the laboratory, shell length (distance 
between anterior and posterior shell mar- 
gins), maximum width (maximum distance 
between lateral shell margins), and height 
(distance between apex and line between an- 
terior and posterior shell margins) were mea- 
sured to the nearest 0.05 mm using calipers 
on 1025 useful, whole shells. Specimens 
were also assigned to either species using 
non-conchological traits, mainly foot mor- 
phology and color (Cretella et al., 1990). At 
Cabo Oropesa, Patella áspera can be easily 
recognized by its pyriform or oval foot, with 
sole yellow or cream with no dark areas. Pa- 
tella caerulea, on the other hand, has an oval 
foot, with sole dark gray or bluish with edge 
and center cream. Use of these diagnostic 
characters resulted in 439 specimens being 
classified as P. áspera and 581 as P. caer- 
ulea. Five specimens could not be unambig- 
uosly assigned to either species and were 
classified as doubtful. Later, the range of 
shell lengths in the total sample (5.30-35.10 
mm) was divided into 31 intervals of 1 mm, 
which were operationally considered as 
growth stages. Specimens were, irrespective 
of their specific identity, grouped into these 
31 shell-length class intervals. 

Because the performance of mixture anal- 
ysis is greatly improved by a large sample 



MULTIVARIATE MIXTURE ANALYSIS IN PATELLIDAE 



35 



size (e.g., Equihua, 1988), only the largest 
subsample was considered for the analysis 
performed in the present study. This sub- 
sample included all specimens with shell 
length between 14 and 15 mm (n = 103). Ac- 
curate measurements of maximum shell 
width and shell height could only be obtained 
from 1 01 of the 1 03 specimens (37 belonging 
to Patella áspera and 64 to P. caerulea) yield- 
ing 101 bivariate data that were submitted to 
the statistical analysis. 

The subsample was considered a mixture 
(superposition of density functions) of two 
components with bivariate normal distribu- 
tion as to maximum shell width and shell 
height. Multinormality of the continuous phe- 
notypic traits in a population is a frequent 
theoretical assumption (HartI & Clark, 1989). 
In a real mixture situation, testing for normal- 
ity would be impossible because group 
membership of the specimens is not known. 
In our sample of classified specimens, multi- 
normality was tested for confirmation. It was 
done for each species separately using (1) 
Kolmogorov-Smirnov goodness-of-fit test 
with Lilliefors correction (Sokal & Rohlf, 1981) 
to test the univariate normality of the mar- 
ginal distributions, and (2) Mardia's test of 
multinormality (Mardia, 1970; Appendix 1) to 
evaluate joint normality. Although marginal 
normality does not imply joint normality, the 
converse is true. Hence, test (1) is useful for a 
fast and easy detection of many types of 
non-normality, whereas test (2) permits eval- 
uation of multivariate normality when results 
of the previous test are inconclusive (i.e., fails 
to reject the hypothesis of normality). 

In the Patella sample case, results of good- 
ness of fit testing revealed no significant de- 
partures from marginal normality and multi- 
normality (P > 0.05) in the growth stage 
(shell-length class interval) that is the focus of 
this report, as well as in most other growth 
stages of either species. 

Statistical analysis of the mixture required 
estimation of 11 parameters, including four 
means, four variances, two covariances, and 
one mixing parameter (proportion of either 
component in the mixture). The estimation 
was accomplished by means of a maximum- 
likelihood approach. The EM algorithm 
(Dempster et al., 1977) was used to compute 
the maximum-likelihood estimates of the pa- 
rameters using the equations studied by 
Wolfe (1970). The procedure has been de- 
scribed by Everitt & Hand (1981) for the gen- 
eral case of a mixture of multivariate normal 



distributions (an arbitrary number of mixed 
distributions and variables, with all parame- 
ters unknown) (Appendix 2). 

This method, although slow, is easily pro- 
grammable and very stable (i.e., shows little 
dependency on the initial estimates of the 
parameters). In the case studied here, includ- 
ing two mixed distributions and two vari- 
ables, the programming was particularly sim- 
ple. Initial estimates of the parameters were 
computed by the program directly from the 
data. The variance/covariance matrices of 
the components were assumed equal to the 
variance/covariance matrix of the mixture, 
and the means were calculated by imposing 
a small deviation (10% of the range of the 
variables) on both sides of the mixture 
means. The means calculated in this way 
were then grouped into vectors taking into 
account the sign of the correlation of the data 
in the mixture. Mixing proportions were set at 
0.5. This approach has proved successful in 
several runs with simulated data. In addition, 
different initial estimates were used in order 
to confirm that the results of the mixture anal- 
ysis did not correspond to a local maximum 
of likelihood (Appendix 2). The convergence 
criterion of the iterative procedure was spec- 
ified in terms of the Euclidean distance be- 
tween successive estimates of the parameter 
vector. Following Everitt (1984), the criterion 
value was set at 0.0001. 

A likelihood ratio test was used to evaluate 
the goodness-of-fit of the mixture (Hassel- 
blad, 1969; Everitt & Hand, 1981; Equihua, 
1988). The statistic is given by 

G = 2 (L, - Lo) 

where Lq is the log-likelihood computed un- 
der the null hypothesis (which assumes only 
one distribution), and L^ is the log-likelihood 
under the alternative hypothesis (which as- 
sumes the mixture of two distributions). Sta- 
tistic G is asymptotically distributed as chi- 
square with degrees of freedom equal to the 
difference in the number of parameters be- 
tween the two hypotheses (six in the present 
case). This approach, however, is not devoid 
of criticisms (Everitt & Hand, 1981; Tittering- 
ton et al., 1985). Under the null hypothesis, 
the mixing proportions fall in the boundary of 
the parameter space, so that conditions for G 
to be asymptotically distributed as chi- 
square are not fulfilled. However, a satisfac- 
tory performance of the test was found by 
Hasselblad (1969) with mixtures of exponen- 



36 



ACUNA & MUÑOZ 



tial, Poisson, and binomial distributions. 
Based on this evidence, Equihua (1988) has 
argued that the likelihood ratio test can be of 
assistance in assessing the number of com- 
ponents in a mixture. 

Once the analysis was completed, the 
probabilities of membership (posterior prob- 
abilities) of each datum (specimen) to each 
component (species) in the bivariate mixture 
were calculated by dividing the component 
density function weighed by its proportion in 
the mixture by the mixture density function. 

The presence of two components in the 
mixture could be taken as evidence of a spe- 
cific discrimination. Alternative interpreta- 
tions based on other phenomena that yield 
mixed distributions in natural populations ap- 
pear rather unlikely. For example, the species 
are hermaphroditic (Bacci, 1947; Fretter & 
Graham, 1976), thus sexual dimorphism is 
not a likely explanation for the presence of 
two components in the mixture. Mendelian 
segregation in the shell dimensions of these 
two species has never been reported, and it 
is likely that, as is the case with other organ- 
isms, traits related to body size are under 
additive polygenic control resulting in a nor- 
mal distribution of maximum shell width and 
shell height (Falconer, 1989; HartI & Clark, 
1989). Also, because the samples were col- 
lected in a uniform environment, a possible 
effect of disruptive selection and/or differen- 
tial reaction seems unlikely. 



RESULTS 

Figure 1 shows scatterplot of the two vari- 
ables measured in the 1 4-1 5 mm shell-length 
growth stage. Inspection does not permit 
discrimination of two components. However, 
the results of the mixture analysis (Table 1) 
suggest the existence of two mixed multivari- 
ate distributions. This can be inferred from (1) 
the absence of an empty component in the 
mixture; (2) the absence of mixing propor- 
tions suggesting a component with a mar- 
ginal representation as could arise from a 
spurious frequency peak in the tails of the 
distribution, and (3) the results of the likeli- 
hood ratio test, which allow rejection of the 
null hypothesis with P < 0.05 (G = 12.72; d.f. 
= 6). Furthermore, the estimated values of the 
parameters indicate a substantial overlap in 
the bivariate distributions for the two compo- 
nents. 

The taxonomic interpretation of the results 




MAXIMUM SHELL WIDTW (mm) 

FIG. 1. Scatterplot for the sample used in the 
present study. Specimens belonging to Patella ás- 
pera are symbolized by closed dots, and those be- 
longing to P. caerulea by open dots. Superim- 
posed lines limit the regions with probabilities of 
membership (posterior probabilities) > 0.95 in the 
components detected through the use of mixture 
analysis. 



TABLE 1 . Results of the mixture analysis. 



Component 1 Component 2 
(Patella áspera) (Patella caerulea) 



Mixing 

proportion 0.45 

Maximum shell 

width mean 10.71 

Shell height 

mean 4.76 

Maximum shell 

width variance 0.35 

Shell height 

variance 0.35 

Maximum shell 

width— Shell 

height covariance 0.04 



0.55 
11.62 
3.88 
0.31 
0.18 

0.07 



of the mixture analysis is straightforward if 
one considers simultaneously the probability 
that each specimens belongs to any one 
component in the mixture and the results of 
their specific diagnosis based on non-con- 
chological traits (Table 2; Fig. 1). When strin- 
gent probability levels are applied (e.g., 0.99 
or 0.95), the classification derived from the 
mixture analysis is congruent with that based 
on non-conchological traits. With few excep- 
tions, the component with the lowest maxi- 
mum shell width mean and the highest shell 
height mean (component 1) corresponds to 
Patella áspera shells, whereas the compo- 
nent with the highest maximum shell width 



MULTIVARIATE MIXTURE ANALYSIS IN PATELLIDAE 



37 



TABLE 2. A comparison of theclassifications arising 
from mixture analysis and from specific diagnosis 
based on non-conchological traits. PM: probability 
of membership in a component; A: number of spec- 
imens ascribed to either component; lA: number of 
incorrect ascriptions; OIA: observed percentage of 
incorrect ascriptions; EIA: expected percentage 
of incorrect ascriptions. 



PM 


A 


lA 


OIA(%) 


EIA(%) 


0.99 


31 





0.00 


1.00 


0.95 


59 


5 


8.47 


5.00 


0.90 


70 


5 


7.14 


10.00 


0.75 


89 


8 


8.99 


25.00 


0.50 


101 


11 


10.89 


50.00 



mean and the lowest shell height mean (com- 
ponent 2) corresponds to P. caerulea shells. 
The number of incorrect ascriptions in- 
creases at low probability levels (e.g., 0.75 or 
0.50), but is always under reasonable values. 
Therefore, it seems safe to conclude that the 
two components detected through the use of 
mixture analysis correspond to P. áspera and 
P. caerulea. 

Although the following discussion is mainly 
based on the analysis of specimens between 
14-15 mm in shell length, the same proce- 
dure was also applied to other shell-length 
class intervals in the sample. Only occasion- 
ally did mixture analysis reveal two compo- 
nents using data from a single interval [e.g., 
18-19 mm (n = 65)]. However, in some cases 
discrimination was accomplished after pool- 
ing data from two successive intervals [e.g., 
1 4-1 5 mm + 1 5-1 6 mm (n = 101 -i- 87), 1 7-1 8 
mm + 18-19 mm (n = 68 -i- 65)]. 



DISCUSSION 

The results of the mixture analysis pre- 
sented here indicate that there are only slight 
differences between the sibling species Pa- 
tella áspera and P. caerulea as far as the bi- 
variate distribution of maximum shell width 
and shell height. The shell of P. áspera is 
slightly narrower and taller than that of P. 
caerulea. It is worth noting that a third vari- 
able, namely shell length, was bearing on the 
results of the bivariate analysis, because the 
specimens were grouped into growth stages 
according to shell length. Therefore, the spe- 
cific differences revealed by the analysis con- 
cern all three variables that determine the 
general shape of the patelliform shells. The 
shell of P. áspera is slightly more oval-conic 



and elevated than that of P. caerulea. This 
difference has been reported in type-materi- 
als for a long time (Bucquoy et al., 1886; 
Christiaens, 1973; Powell, 1973) and is po- 
tentially interesting, because shell shape is a 
taxonomic trait that was extensively investi- 
gated in relation to adaptive value (Segal, 
1956; Lowell, 1984). 

The discrimination between Patella áspera 
and P. caerulea extends the results of a pre- 
vious report (Muñoz & Acuña, 1994) and il- 
lustrates the use of multivariate mixture anal- 
ysis to deal with situations in which several 
traits with overlapping variation are used for 
classification. Multivariate mixture analysis 
proved capable of discriminating between 
these two species in spite of a substantial 
overlap in the mixed distributions and a mod- 
erate sample size. We hope that these results 
will encourage the use of multivariate mixture 
analysis among taxonomists. 

Moreover, mixture analysis seems prefera- 
ble in many taxonomic applications to other 
statistical procedures, such as discriminant 
analysis and ordinary cluster analysis (Flury 
et al., 1992). Mixture of distributions arise 
when a population is subdivided into homo- 
geneous components, but it is unknown from 
which of the components any given observa- 
tion originates. Mixture analysis models this 
situation, attempting to estimate the statisti- 
cal parameters of the components and their 
proportions In the population by means of a 
sample of unclassified observations. Later, 
the observations can be classified using the 
parameter estimates. In discriminant analy- 
sis, the basic problem is to assign a given 
observation to one of two or more classes on 
the basis of the value of this observation. The 
procedure requires reference samples with 
known group membership. Ordinary cluster 
analysis attempts to partition the data into 
homogeneous subgroups without consider- 
ing a statistical model and assuming that the 
subgroups are distinct and do not overlap. 
Therefore, mixture analysis seems preferable 
for dealing with taxonomic problems in which 
(1) the statistical distribution of traits is used 
for discrimination, (2) overlapping variation is 
present, and (3) reference samples are not 
available. In these situations, mixture analy- 
sis is a reasonable alternative provided that 
the number of variables (and therefore pa- 
rameters that need estimation) does not de- 
mand an inordinate sample size. When the 
number of variables is high, such methods as 
principal component analysis can be used to 



38 



ACUNA & MUÑOZ 



reduce the dimensions of the variability to a 
smaller number of meaningful and indepen- 
dent variables. 

However, a general discussion of the 
methodological implications of mixture anal- 
ysis is necessary. In particular, application of 
mixture analysis to the problem of species 
discrimination entails a risk of misinterpreta- 
tion. The coexistence of populations leads, 
indeed, to mixtures of distributions, but other 
phenomena may be responsible for the pres- 
ence of mixed distributions in populations. 
Mendelian segregation, sexual dimorphism, 
disruptive selection, and multiple environ- 
mental reaction are examples of potential 
sources of mixed distributions. Thus, mixture 
analysis, like other more popular statistical 
techniques, should be not be considered as 
an alternative, but rather as an aid to tradi- 
tional taxonomic methods. 



ACKNOWLEDGMENTS 

We are very grateful to J. D. Bermúdez (De- 
partamento de Estadística e Investigación 
Operativa, Universidad de Valencia), E. Font 
(Departamento de Biología Animal, Univer- 
sidad de Valencia), and M. Sendra (Departa- 
mento de Estadística e Investigación Opera- 
tiva, Universidad de Valencia) for providing 
useful information and discussion of an ear- 
lier draft of this manuscript. We also thank R. 
T. Dillon and an anonymous referee for stim- 
ulating discussion and constructive criticism. 



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BUCQUOY, E., PH. DAUTZENBERG & G. F. DOLL- 
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CERVELLA, P., L. RAMELLA, С. A. ROBOTTI & G. 
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FISCHER-PIETTE, E. & J. M. GAILLARD, 1 959, Les 
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MARDIA, K. v., 1970, Measures of multivariate 
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MULTIVARIATE MIXTURE ANALYSIS IN PATELLIDAE 



39 



MCLACHLAN, G. J. & K. E. BASFORD, 1988, Mix- 
ture models. Marcel Dekker, New York. 253 pp. 

MUÑOZ, M. A. & J. D. ACUÑA, 1994, On the tax- 
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Revised Ms. accepted 17 January 1995 



APPENDIX 1 

Mardia's Test of Multinormality 

Mardia's test is a simple but useful test of 
multinormality (Mardia, 1970). If y-,, . . . , y^ 
are a random sample of k-dimensional data 
from a normal multivariate distribution of y, 
the sample estimators of skewness and kur- 
tosis, bi and bj, are 

n n 

bi = 1/n'XE['yh-y)'S-My, -y)f 



b2=1/n^ [(y, -y)'S-^ (y, -y)f 

1=1 

v\/here у is the sample estimate of the mean 
vector and S is the sample estimate of the 
variance/covariance matrix. Then, for large 
samples, we have, asymptotically, 

A=1/6nbi-~x? f = 1/6k(k+ 1)(k + 2) 



В 



k(k + 2) 



Ni(0,1) 



[8k(k + 2)/n]^/2 

Although these distributions are only ap- 
proximate for moderate sample sizes, they at 
least indicate whether the data show any 
marked departure from multivariate normal- 
ity. 

APPENDIX 2 

Maximum Likelihood Estimation of the 
Parameters of a Mixture of Multivariate 
Normal Distributions by Means of the 
EM Algorithm 

If C-,, . . . , Cg are the g components 
with multivariate normal distribution which 
contribute to the mixture in proportions 
Pi, ..., Pg respectively, < p¡ < 1 



Îp. = i 



and fj (y) is the probability density function of 
the distribution of y ~ N,, (m,, SJ in C, (i=1, 
. . . , g) given by 

f,(y) = I 2jrS, I -^^^ 

exp[-1/2(y- m¡)'Sr^ (y- mj)] 

then, considering a random sample of n k-di- 
mensional data У-,, . . . , Уп the density of y^ is 
given by 



f(yi) = £p,f,(y,) 



:1, ..., П) 



and the maximum likelihood estimates of the 
parameters of the mixture (Everitt & Hand, 
1981) are given by 



p, = ^Wi/n (1=1,... ,g) 



m, = 2^ w,j y, /n p, 



S,= 



where 



(i=1, 



m, 



Y^ w„ (y, - m,) (y, - 
Lj=i 

(i=1,..., g) 



Wi, = p¡fi(yj)/5^Prfr(yj: 



/np, 



(1) 

(2) 
(3) 



(i=1, ..., g;j=1, ..., n) 



40 



ACUNA & MUÑOZ 



Equations 1 through 3 are solved itera- 
tively. Initial estimates of the parameters are 
used in the right hand side of the equations to 
obtain other estimates of the parameters op- 
erating the data. The resulting estimates are 
then used in the right hand side of the equa- 
tions to yield new estimates, and so on. The 
iterative procedure continues until two suc- 
cessive estimates of the parameters differ 
only by some arbitrarily small amount. 

As is the case with other iterative pro- 
cesses, with the EM algorithm there is no 
guarantee that the global maximum of the 
likelihood function will ever be found. It is 
possible that, depending on the initial esti- 



mates of the parameters, one or several local 
maxima might result. In these instances, the 
solution with the largest likelihood would be 
accepted. However, EM algorithm shows, 
compared to other algorithms, little depen- 
dency on the initial estimates of the parame- 
ters (Everitt, 1984). 

Note: A copy of the program written to 
compute the maximum likelihood estimates 
of the parameters of a mixture of two bivari- 
ate normal distributions is available from the 
authors upon request. This program is writ- 
ten in Quick Basic and runs on IBM PC or 
compatible computers. 



MAU\COLOGIA, 1995, 37(1): 41-52 

THE LIFE CYCLE, POPULATION DYNAMICS, GROWTH AND SECONDARY 

PRODUCTION OF THE SNAIL VIVÍPAROS CONTECTUS (MILLET) 

(GASTROPODA: PROSOBRANCHIA) IN THE MARSHES OF THE RIVER 

STRYMONAS, SERRES, MACEDONIA, NORTHERN GREECE. 

N. Eleutheriadis & M. Lazaridou-Dimitriadou 

Section of Zoology, Department of Biology, University of Thessaloniki 54006, 

Thessaloniki, Greece 

ABSTRACT 

The life cycle, population dynamics, growtin and secondary production of the prosobranch 
freshwater snail Vivíparas contectus were studied in the marshes of Strymonas River upstream 
of its entry into the artificial Lake Kerkini, Serres, Macedonia, northern Greece. Demographic 
analysis of the population of V. contectus revealed that two or more generations existed in the 
field throughout the year. The sex ratio was 1:1. Reproduction took place in the beginning of 
spring or at the end of autumn, depending on the water level and water temperature in the study 
area. Growth of newly born individuals mainly took place during spring and early summer. Von 
Bertalanffy's method suggested that V. contectus may live up to five years to reach its maxi- 
mum possible size (51 mm). Annual secondary production, calculated by Hynes' size frequency 
method, revealed a mean annual density of three individuals/m^, a mean standing crop (B) of 
4.19 g dry body weight/(m^.year), and an annual production (P) of 13.45 ± 12.9 g dry body 
weigh/(m^.year). Annual turnover ratio (P/B) was 3.21 and turnover time was 113.7 days. 

Key words: Viviparus contectus, Gastropoda, ecology, population dynamics, production. 



INTRODUCTION 

Viviparus contectus is a prosobranch snail 
found in the marshes of Strymonas River 
(old bed of Stn/monas River) upstream of its 
entry to Lake Kerkini, which lies 100 km from 
Thessaloniki in Serres, Macedonia, northern 
Greece. These marshes were formed in 1982 
after the construction of a new bed of Stry- 
monas River parallel to the old one. The lake 
is an artificial water storage reservoir, con- 
structed on the site of a natural marsh and 
small natural lake. The area of the lake is in- 
cluded in the list of the internationally impor- 
tant wetlands, edited by the United Nations 
at Ramsar in 1971. It supports a numerically 
rich, diverse wildlife (Pelecanus onocrotalus, 
P. crispus, Hirudo medicinalis), including V. 
contectus. 

Studies on the biology and ecology of fam- 
ily Viviparidae occurring in freshwater show 
considerable differences between genus, 
species and populations (Stanczykowska et 
al., 1 971 ; Samochwalenco & Stanczykowska, 
1972; Young, 1975; Bernardi et a!., 1976; 
Browne, 1 978; Vail, 1 978; Jokinen et al., 1 982; 
Ribi & Gebhardt, 1986). Studies of these dif- 
ferences can provide worthwhile insights into 
the strategies that the species follow (Young, 
1975). 



Although the prosobranch snail Viviparus 
contectus (Millet) is widespread in Europe 
(Zhadin, 1952), little is known about its life 
history, apart from studies done by Samoch- 
walenco & Stanczykowska (1972) in Poland. 
It is one of the most important constituents in 
the food web of lake fauna and also the main 
intermediate host of trematode parasites. 
This gastropod is relatively large and is nu- 
merically and functionally a dominant mem- 
ber of the second trophic level of the macro- 
fauna of Lake Kerkini. Consequently, a study 
on the life cycle, population dynamics, 
growth, and secondary production of this 
prosobranch snail was considered valuable. 



MATERIALS AND METHODS 

The abiotic characteristics of the study 
area have been studied in detail, including 
water level, precipitation, water temperature, 
pH, dissolved oxygen, chloride, water hard- 
ness, and PO4-P, in relation to the density 
and growth of V. contectus (Eleutheriadis & 
Lazaridou-Dimitriadou, in press.). Presented 
here are the water level of Lake Kerkini at 
weekly intervals during the study period (Fig. 
1), which affects the marshes around the lake 



41 



42 



ELEUTHERIADIS & LAZARIDOU-DIMITRIADOU 




j F MÂMJ J ASÓÑDJFM AM J j ÁSÓÑ DJ FMAMJJASÓÑd' 
1989 1990 1991 

Months 



FIG. 1. Water level at weekly intervals of artificial Lake Kerkini during the years 1989, 1990 & 1991. 



where this snail lives, monthly water temper- 
atures (Fig. 2) at the marshes, and monthly 
changes of the concentration of dissolved 
oxygen (Fig. 3), at the marshes, which seem 
to affect the onset of hibernation and repro- 
ductive period of this species. 

The study started in October 1989 and 
lasted for two years. Data from October 1 989 
to August 1991 were used for the demo- 
graphic analysis of the populations of I/, con- 
tectus, which dominate the benthic, littoral 
and sublittoral fauna. Samples were taken 
using random coordinates (Lewis & Taylor, 
1972) by use of a net "drag" based on the 
Doulkeite sampler (illustrated in Lammote & 
Bourlière, 1971) with a 1-m^ surface, at ap- 
proximately monthly intervals throughout the 
year. Vegetation, debris and snails were hand 
washed through 1-mm mesh sieves. Snails 
were sexed (males have an enlarged right 
tentacle used as a copulatory organ), mea- 
sured and then returned as near as possible 
to their initial places. 

Measurements of the distance between 
the apex of the shell and the farthest point on 
the aperture (shell height) were made using 
vernier calipers. In addition to the shell height 
(H) of each specimen, the largest shell diam- 
eter (D) and the perpendicular diameters of 
the peristome (d & a) were also measured to 
the nearest 0.1 mm. 

The total number of samples were deter- 



mined so that the percentage error (Table I) 
was not more than 25% (Elliott, 1971). 

Spatial distribution of the snails in the hab- 
itat was examined by using Taylor's (1961) 
power law. The parameter b from Taylor's 
equation s^ = ax*^ (where a = constant, s^ = 
variance, x = mean number of snails found in 
a sample unit, a and b = constants) was used 
as an index of dispersion. Parameter b is 
fairly constant and characterizes a species 
(Southwood, 1966); it is independent of the 
total number of samples and the total num- 
ber of animals in the samples but is affected 
by quadrat size (Elliott, 1971). 

The class interval of the monthly size-fre- 
quency histograms of shell height (H) was 3 
mm, as determined by Goulden's method 
(Cancela da Fonseca, 1965). Cohorts were 
separated using probability paper (Harding, 
1949). This method was valid because the 
modes of the age classes were separated by 
at least 2.5 standard deviations (Grant, 1989). 
Although some age classes had less than 50 
individuals, the modal values were consistent 
from month to month, which confirms that the 
modes were real and not the result of sam- 
pling variation. This method has been used for 
demographic analyses of the populations of 
other molluscs (Hughes, 1970; Lévèque, 
1972; Daguzan, 1975; Lazaridou-Dimitriadou, 
1981; Lazaridou-Dimitriadou & Kattoulas, 
1985; Staikou et al., 1988, 1990, 1991). 



LIFE CYCLE OF VIVIPARUS CONTECTUS 



43 



40-, 
30 
20-1 
10- 








-#- 




Ш 



Ш 




8 10 
1989 



4 6 8 10 12 2 4 6 8 10 12 2 4 
1990 ,. 1991 1992 



Months 
FIG. 2. Monthly water temperatures at the marshes of Strymonas River from July 1989 to April 1992. 



20-, 



10- 



^ 




b 



Ы 



i 




Ш 




10 



1989 



4 6 8 10 12 2 4 6 8 10 12 2 4 

1990 ., ,, 1991 1992 

Months 



FIG. 3. Monthly concentrations of dissolved oxygen (D.O.) at the marshes of Strymonas River from July 
1989 to April 1992. 



For the study of absolute growth, data 
from the modal distribution of V. contectus 
were used (e.g., the growth of one age class 
was followed by the growth of the same age 
class the following month taking into consid- 
eration that time intervals always had to be 
equal). For determination of the theoretical 
growth curve, Bertalanffy's (1938) equation 
was employed: H, = H^^^ [1 - e^^<'"*°>], 
where Н^ = the largest shell height at age t, 
Umax = 'the asymptotical maximum possible 
largest shell height, К = growth rate coeffi- 
cient, t = time in months, and to = hypothet- 
ical time when H is equal to "zero." 

The coefficient К and H^^ax were deter- 
mined according to Walford's (1946) method. 
Hmax is ^he intersection point of the growth 
curve H,^-, = f(Ht) and the line drawn at 45" 
through the zero point. The coefficient К is 
equal to -loga* 2,30259 (where a = the slope 
of Walford's line). For the determination of 
the date of birth of an age class on the time 
axis, it is possible to use a secondary origin 



(f = 0) corresponding to the smallest snails 
found in the biotope during the study period 
of a species (in our case was H = 5.5 mm), 
assuming that all the small snails of this spe- 
cies have been captured with the same size 
and that all age classes follow the same 
growth laws. Consequently, it is possible to 
draw the theoretical growth curve of shell 
height in relation to time from the first capture 
Hf = H^a^ [1 - e"*^**' '°\ If the shell height 
at the moment of birth is known from labora- 
tory data (in our case was H = 3.5 mm), the 
axes may be changed taking as origin birth 
(zero point) (to = t'-t"). So Bertanlaffy's 
equation becomes Hj = H^^ax [1-e^'' *°*], 
and the life span of the studied species until 
H^^ax can be estimated. 

For the study of relative growth, the mor- 
phometric criteria of shell diameter (D) in re- 
lation to the perpendicular diameters of the 
peristome (d & a) were used from all the an- 
imals sampled during 1990 (Table I). Mayrat's 
method (1965 a, b) was used to compare the 



44 



ELEUTHERIADIS & UXZARIDOU-DIMITRIADOU 



growth of the shell diameter (D) in relation to 
the peristome surface (Pg) between immature 
and mature male and female snails. Because 
the peristome was almost an ellipse, its sur- 
face area (Pg) could be calculated by the for- 
mula: (P3) = 3.14 • d ■ a. 

Annual production in 1990 was calculated 
by the size-frequency method, because it 
has an important advantage in that single co- 
horts need not be identified to calculate pro- 
duction (Krueger & Martin, 1980), although it 
may produce an overestimate (Waters & 
Crawford, 1973). This method has been used 
for the determination of gastropod produc- 
tion, because it gives similar results to those 
obtained by Russell-Hunter's (1970) method. 
Both methods have been compared for B. 
graeca (Eleutheriadis & Lazahdou-DJmitha- 
dou, submitted). The formula as modified by 
Benke (1979) and Krueger & Martin (1980) 
can be written as: 



mature shells (mature: H > 17 mm and imma- 
ture: H < 17 mm, according to the study of 
relative growth) with 5N HCl, as described in 
Staikou et al (1988). Size classes >18 mm 
contained two females and two males (ex- 
cept for the last size class, which contained 
only females), in the sex ratio 1:1 as in nature, 
and in the size classes from 3 to 18 mm 20 
snails were examined (in total 60 snails). 

On March 1991, some females were re- 
turned to the laboratory for observations on 
birth. There the mean number of new-born 
snails released per female was determined. 
We also measured the mean shell height of 
new-born snails. The differentiation of the 
genitalia in relation to the age of the snails 
was also studied under a stereoscope. The 
maturation of sectioned female and male go- 
nads in relation to the age of the snails were 
studied under a light microscope. 



P=a 



^Z (n,-n,^i)tW, -Wi.i) 



0.5 



+ (naXWg 



365/CPI, 



where P = the mean annual production in mg, 
a = number of size classes, ñ] = number of 
snails at the size class j in number, Uñj = 
variance of ñ^, W^ = mean individual dry body 
weight+mean dry shell of organic material (in 
mg), and CPI = cohort production interval in 
days. 

For the determination of the variance (U) of 
P the following formula was used: 



U(P)=a2 

+ (Wa-Ga-i)^U(n 



Gf U(ni)+ Z (G,-G|_i)^U(n|) 



(365/CPI)2, 



where Gj = geometric mean of weight of pairs 
of successive size classes. For the determi- 
nation of ñj and Uñ|, data from the population 
dynamics of V. contectus were used and 
snails collected during 1990 were grouped 
into 15 size classes of 3-mm intervals. 

To determine dry body weight and the dry 
organic shell material, 60 snails representing 
all size classes were brought to the labora- 
tory in April 1990, where their shell height (H) 
was measured in mm and they were dried in 
vacuo at room temperature; dry body weight 
(W) in mg was measured one week later. Dry 
organic shell material was also estimated af- 
ter successive treatments of immature and 



RESULTS 

Aspects of the Biology 

The snails were sexually mature when the 
largest shell height (H) exceeded 17 mm, as 
verified by following gonad maturation. Ma- 
turity was attained three months after birth if 
the new-born appeared in early spring, but 
eight months if they appeared in autumn. The 
sex ratio in the three consecutive years of 
study (1989, 1990, 1991) was equal to 1:1. In 
1989, new-born snails appeared in October 
when water level was high (Fig. 1) and the 
water temperature was > IS'X (Fig. 2). In the 
same season in October 1990, because wa- 
ter level was low (Fig. 1) and water tempera- 
ture < 15" С (Fig. 2), females carried fully 
formed embryos through the winter and gave 
birth during spring 1991. No females smaller 
than 16 mm shell height contained develop- 
ing embryos. The mean number of new-born 
snails released per female was 16 ± 8.8 (n = 
8) and the new-born snails had a mean shell 
height 5.15 ± 0.58mm (n = 61). Fully devel- 
oped young were found throughout the year 
in the brood sacs of the adult females. Fe- 
males attained larger sizes because of their 
greater longevity. The snails in this popula- 
tion were active during spring, summer and 
until the end of autumn. At the end of autumn 
and during winter, snails were buried in the 
mud of deeper water (1-2 m). The population 
began to move into shallower waters by early 



LIFE CYCLE OF VIVÍPAROS CONTECTUS 



45 



TABLE 1. Viviparus contectus population density in the marshes of Strymonas River from July 1989 to 
August 1991 (n: number of samples; x: mean number of animals/m^; s: standard error). 











1989 














6/7 


21/7 


2/8 


17/8 


20/9 


2/10 


19/10 




n 

X 

s 

Percentage error D 


40 
0.75 
0.26 

34.6 


31 
1.52 
0.38 

25.2 


38 
1.26 
0.25 

20.0 


33 
1.12 
0.29 

26.3 


22 
2.45 
0.50 

20.3 


28 
1.53 
0.34 

22.1 


40 
0.77 
0.17 

22.4 














1990 










22/4 


13/5 


26/5 


10/6 


29/6 


21/7 


4/8 


29/8 


13/9 


n 

X 

s 
Percentage error D 


28 

1.64 
0.48 
29.7 


24 
2.7 
0.45 

16.7 


24 
2.5 
0.43 

17.5 


24 
3.29 
0.67 

20.1 


24 
2.62 
0.61 

23.4 


20 
1.2 
0.34 

28 


24 
2.91 
0.47 

16.5 


16 
2.75 
0.6 

21.6 


16 
2.68 
0.53 

19.7 






1990 










1991 








24/9 


22/10 


7/11 




24/3 


21/4 


16/5 


3/6 


26/6 


n 

X 

s 

Percentage error D 


16 
2.5 
0.74 

28.9 


22 

1.59 
0.48 
30.5 


24 
1.41 
0.37 

25.8 




14 
4.78 
1.02 

21.4 


8 

8.75 
2.23 
25.5 


16 

3 

0.6 
19.2 


15 

2 

0.47 
22.8 


21 

2 

0.32 
16.1 






1991 


















12/7 


1/8 


24/8 




n 

X 

s 

Percentage error D 


15 
2.4 
0.52 

21.4 


11 
1.3 
0.56 

32 


14 
2.43 
0.83 

34 





spring and occupied the highest 50 cm of 
water. Migration to deeper waters occurred 
again between October and November, so 
that over-wintering of all members of the 
population occurred in water of 1-2 m depth. 

Population Density and Spatial Distribution 

Population density fluctuated during the 
study period, either from month to month or 
from year to year (Table 1). Low values ap- 
peared in July and in the end of autumn each 
year, whereas high values were recorded in 
March and AphI in 1991. The mean popula- 
tion density of V. contectus during the study 
period 1 989-1 991 was 2.84 ± 2 (mean ± stan- 
dard deviation) snails m ^. 

The spatial distribution of V. contectus was 

found to be contagious, because parameter 

b of Taylor's power law was equal to 1 .43 (s^ 
= 1.71x^^3^ 



Demographic Analysis of the Population of 
V. contectus 

The analysis of size frequency histograms 
(Fig. 4) from October 1989 to April 1991 with 
probability paper showed the following (Fig. 
5): 

(a) Two cohorts were found in the habitat 
throughout the year; a third was added after 
the release of newly born individuals. 

(b) In 1989, the newly born individuals ap- 
peared in mid-autumn and in 1991 the new- 
born appeared in the beginning of spring. 

(c) Increased growth rate for newly born 
young occurred during spring and in the be- 
ginning of summer. Growth was continuous 
until the end of autumn. 

(d) One year after the new-born appeared, 
the largest shell height was about 28 mm; 
two years later, the snails were about 35 mm 
(March 1991) and the third year about 37-40 

mm (Ggg). 



46 



30 
20- 

lo- 
ci 



ELEUTHERIADIS & LAZARIDOU-DIMITRIADOU 

10/89 30-, „, 8/90 



i 



\n. . X\nn.\ 



30 
20 
10-1 



% 



Полл, oi ПлШЛ 



40-1 
20 



Ша ol ■ ■ ■ л. 



% 



П 5/91 



п. ■ .плЛЛЛ. ■ 



о 6 12 18 24 30 36 42 6 12 18 24 30 36 42 6 12 18 24 30 36 42 



40 

20 

О 



4/90 



30 
20 
10 



1 . . л . '-'Л . п . Цпл . а 



9/90 



п1 



1Д1 



30-, 
20- 

10 



Un, а 



■ ■ ■ ■ .П.! 



6/91 



Л . п ,1 Inj IJ 1 л , 



О 6 12 18 24 30 36 42 6 12 18 24 30 36 42 6 12 18 24 30 36 42 



20-, 


% _. 


5/90 




30-, 


10- 

п- 


^.пДц., 


--дЦ- 


п 


20- 

10- 

д а 



11/90 „ 



пП1 



40 

30-1 

20 

10 



% 



8/91 



['"а DJ 



ЛллПлаП 



О 6 12 18 24 30 36 42 6 12 18 24 30 36 42 6 12 18 24 30 36 42 

D (mm) 
3/91 



30-, 


% 


6/90 




40-, 


% г. 






-. 


.40- 




■А)- 


г 












Г| 




20- 




1U- 
0- 


п 


-Цпди 


До, 


10- 

а 





--рР. 



[Од 



30. 
20 
10 



О 6 12 18 24 30 36 42 6 12 18 24 30 36 42 

»/о 7/90 60-, о/, ^ 4/91 

40-1 
20. 



Loi 



ш i 



J 



U . . r, . r. . Л , г.Л , пЛ .-. 



о 6 12 18 24 30 36 42 6 12 18 24 30 36 42 

FIG. 4. Size frequency histograms of Viviparus contectus in the marshes of Strymonas River from October 
1989 to August 1991. 



45-. 

40- 
35- 
30- 

"e 25- 

E 

I 20. 

15. 

10. 

5. 



Hibernation 



20%I15% 



30% 




55% 



T — 77—1 — " — I — ■ — I — ■ — r 

10/89 4/90 5 6 7 



-I — ' — Г- 

8 9 



10 11 
Months 



■ft- 



3/91 



FIG. 5. Population analysis of the populations of Viviparus contectus at marshes of Strymonas River from 
October 1 989 to August 1 991 . Percentages denote the contribution of each cohort to the total population. 
(G88 to G91 indicate when a generation started and when it ended). Dotted lines represents a decrease in 
shell height (H) because of the death of the largest individuals. 



LIFE CYCLE OF VIVIPARUS CONTECTUS 



47 



TABLE 2. Estimation of statistical parameters of the population of Viviparus contectus 
[where a,b: constants, r: coefficient correlation, N: number of snails, D: the mean shell 
diameter, Ps: 1/10 d • a, (d, a = the perpendicular diameters of the peristome, g: standard 
deviation)] from Teissier's regressions. 



Data 


Entire sample 


immature snails 


mature snails 


a ± G 


0.511 ±0.037 


0.421 ±0.012 


0.556 + 0.0055 


logb ± G 


0.657 ± 0.047 


0.735 ± 0.008 


0.594 ± 0.007 


г2 


0.957 


0.937 


0.932 


logDlG 


1.304 ±0.137 


1.019±0.10 


1.333 ±0.103 


logPs ± G 


1.266 ±0.268 


0.673 ± 0.235 


1.326 ±0.186 


N 


819 


75 


744 



Relative Growth 

The study of the relative growth of D in 
relation to Pg (for practical reasons we used P^ 
as 1/10 • d • a) showed a positive correlation 
between D and P3 (r^ = 0.957, n = 81 9) (Fig. 6). 
Knowing that gonad differentiation was com- 
plete (first appearance of spermatozoa and 
mature oocytes) when the largest shell diam- 
eter reached 13.5 mm (corresponding to 17 
mm shell height), it was decided to examine 
whether relative growth rate was the same in 
the two size groups, that is those with D < 1 3.5 
mm and those with D > 13.5 mm. A logarith- 
mic transformation was applied to the data 
because the coefficient of correlation was 
higher than for raw data (0.957 and 0.950 re- 
spectively). A statistical difference (P < 0.01) 
was found between the slopes of the two re- 
gression lines using Mayrat's method (1965a, 
b) (Table 2). The intersection point of the two 
regression lines, corresponded to D = 14.9 
mm, near to the size that sexual maturity was 
attained (Fig. 6). No statistical difference was 
found between the regression lines of mature 
female and male snails. 

Absolute Growth 



that the minimum H of new-born snails was 
about 3.5 mm and their age t", the age from 
zero point to = (f - t") was calculated. By 
starting the curve at birth (zero point), when 
snails had their smallest H (equal to 3.5 mm), 
the theoretical growth curve of H in rela- 
tion to age was calculated: Н( = 52.3 



[1 



,-0.06(t+1.17)' 



]. From this curve (Fig. 7), it 



was found that V. contectus may live up to five 
years before reaching its maximum size ac- 
cording to Von Bertalanffy's equation. 

Secondary Production 

The calculations of the size-frequency 
method are listed in Table 3. The mean bio- 
mass of each size class is expressed in dry 
weight. 

Applying Benke's correction, values of n 
(mean annual density), В (mean annual crop) 
and P (annual production) were calculated to 
be 3 individuals/m^, 4.19 g dry body weight/ 
m^.year and 13.45 ± 12.9 g dry body weight/ 
m^.year respectively. The annual turnover ra- 
tio P/B was 3.21 and the turnover time was 
113.7 days. 



Knowing that after maturity growth rate was 
the same between male and female V. con- 
tectus, we decided to study absolute growth 
in all snails. H^g^, which represents the inter- 
section point of Walford equation of a straight 
line (Ht^i = 0.941 H, + 3.087) and the diagonal 
И^ = H,^i, was 52.3 mm. By using the slope of 
the line (a = 0.941), which showed the growth 
rate of the animals, the coefficient К was cal- 
culated as 0.06. Knowing the minimum H of 
the measured snails in the biotope during the 
study period (H = 5.5 mm), the growth of the 
snail shell height was calculated by Bertalan- 
ffy's equation Н^- = 52.3 [1-е oo6(t4i.84)-| 
Because it was known from laboratory data 



DISCUSSION 

Populations of Viviparldae from various 
habitats appear to differ in a number of life 
history traits. Intraspecific and interspecific 
differences exist in size of new-born snails, 
number of broods/year, size of largest males 
and females, time of birth, and life span of 
females (Chaberlain, 1958; Samochwalenko 
& Stanczykowska, 1972; Young, 1975; Ber- 
nardi et al., 1976; Browne, 1978; Vail, 1978; 
Jokinen et al., 1982; Buckley, 1986; Ribi & 
Gebhardt, 1986). Viviparus contectus is iter- 
oparous and viviparous. Birth begins in mid 
autumn or in the beginning of spring. Spring 



48 



ELEUTHERIADIS & LAZARIDOU-DIMITRIADOU 




Ps=10.9 mm 



FIG. 6. Relative growth of the shell diameter in relation to Ps of shell peristome in the whole population and 
in mature and immature snails of Viviparus contectus (Teissier's regression lines). 




"з5 3^ 

Months 
FIG. 7. Theoretical growth curve of Viviparus contectus. 



48 



54 



reproduction is also reported for other spe- 
cies of the Viviparidae by Van Cleave & Cham- 
bers (fronn Vail, 1978), Van Cleave & Altringe 
(from Vail, 1978), Chaberlain (1958), Fretter & 
Graham (1962), Young (1975), Bernardi et al. 
(1 976), Browne (1 978), Vail (1 978) and Jokinen 
et al. (1982), possibly because in this season 
the environmental conditions favour survivor- 
ship and rapid growth of the new-born snails. 
In contrast to most other molluscs, fecundity 
of V. contectus is low, reflecting the conse- 
quences of viviparity, as has also been re- 
ported for V. georgianas by Browne (1978). 



The number of new-born snails released per 
female is variable. This number in the genus 
Viviparus ranges from 2.5 to 90 snails. In 
Poland, V. contectus released 4.5-10.2 
new-born snails per female (Samochwalenco 
& Stanczykwoska, 1972), whereas in our 
study, the number of newborn snails was 16 
± 8.8 (n = 8). Selection probably drives female 
toward a larger size than males as a conse- 
quence of the cost of viviparity. The repro- 
ductive output of smaller females is not only 
limited bioenergetically, but smaller size 
places severe physical constraints on the 



I 



LIFE CYCLE OF VMPARUS CONTECTUS 



49 



TABLE 3. Calculation of production of Viviparus contectus by the size-frequency method. Annual 
production based on sets of samples from April 1990 to April 1991 (where ñ, = number of snails at the 
size class j in number; Un, = variance of ñ,; W, = mean individual dry body weight+mean dry shell of 
organic matter (in mg); G, = geometric mean of weight of pairs of successive size classes; В = mean 
standing crop or population biomass in mg; P = annual production in mg; P/B = annual turnover ratio; a 
= number of size classes; CPI = cohort production interval. 













(B) 


P' 


Class 








__G, 


[ñjWj] 


(ñ, ñ,.,)(G,) 


range 


n, /m^ Un, 


n, n,,, 


W, (mg) 


(W,W„,)°' 


(mg m^) 


(mg m^) 


3-6 


0.42 0.0224 


-0.04 


0.042 


64.8 


17.5 


-2.5 


6-9 


0.45 0.6475 


0.22 


0.100 


154.3 


45.4 


34.7 


9-12 


0.23 3.7573 


0.19 


0.238 


310.9 


54.6 


58.1 


12-15 


0.04 0.0157 


-0.01 


0.406 


483.2 


17.3 


-7.1 


15-18 


0.06 0.0023 


-0.06 


0.575 


653.2 


33.0 


-39.9 


18-21 


0.12 0.0196 


-0.01 


0.742 


821.7 


87.9 


-12.0 


21-24 


0.13 0.0191 


-0.01 


0.910 


990.4 


121.1 


-8.7 


24-27 


0.14 0.0047 


-0.02 


1.078 


1217.9 


153.0 


-18.8 


27-30 


0.16 0.0469 


-0.03 


1.376 


1604.1 


216.5 


-4.9 


30-33 


0.19 0.0240 


-0.12 


1.870 


2087.8 


351.3 


-250.3 


33-36 


0.31 0.0975 


-0.09 


2.331 


2545.6 


717.4 


-219.1 


36-39 


0.39 0.0554 


0.14 


2.780 


3069.9 


1094.9 


420.8 


39-42 


0.26 0.0897 


0.18 


3.390 


3668.6 


870.4 


659.1 


42-45 


0.08 0.0185 


0.05 


3.970 


4222.0 


306.0 


225.9 


45-48 


0.02 0.0013 


0.02 


4.490 


4490.0 


105.9 


105.9 


365 days 


3 


4192.1 mg/m^ 


897 


P = a-P'-365/CP 


1 = 15-897-365/365 = 


13455 mgm 


2 or 13.455 gm" 


"^ in 365 days. 


U(P) = Uñ,(G,G,_i)2 


■ (365/CPI)2 • a^ = 


41730400 














Confidence limits of P = P + 2-[U(P)° ^ 


■] = 13.455 ± 


12.92 








P/B= 13.455/4.192 = 3.21 












Turnover time = 


113.7 days 













number of embryos that can be maintained In 
the uterus if discrete embryo size units are to 
be maintained. By contrast, males following 
the strategy of attempting to mate with as 
many females as possible would have only 
limited time for feeding, resulting in slow 
growth and a much shorter life span than fe- 
males. This has also been reported for V. 
georgianos by Browne (1978). 

Viviparus contectus in Lake Kerkini under- 
take distinct seasonal migrations into deeper 
water in November following the drop in 
marsh temperatures, and they migrate back 
into shallow water in early spring. Although 
other species of Viviparidae appear to mi- 
grate before a decrease in temperature 
(Stanczykowska & Magnin, from Jokinen et 
al., 1982), the decline in temperature appears 
to trigger a migration of V. contectus into 
deeper water in the marshes, bringing the 
snails from summer feeding areas into the 
hibernation area of 2 m depth. Snails migrate 
to avoid areas of low temperatures (Skoog, 
1971; Horst & Costa, 1975; Vincent et al., 
1981) and unfavourable ecological condi- 
tions in the surface water (Coulet & Alfaro- 



Tejera, 1985). Other factors that provoke mi- 
gration might be seasonal habitat changes 
(Lilly, 1953; Jokinen, 1985), changes in water 
level (Skoog, 1971), food availability (Russell- 
Hunter, 1953), or water currents that flow 
faster as vegetation dies back (Lilly, 1953; 
Fretter & Graham, 1962; Boss et al., 1984; 
Lodge et al., 1987). Additionally, snails mi- 
grate to areas of macrophytic vegetation as a 
preferred habitat for the release of new-born 
snails or egg deposition, as shown ior Amní- 
cola limosa by Horst & Costa (1975). The re- 
cruitment of newly born snails to the popula- 
tion during the breeding season in March and 
April 1 991 was the main reason for the rise in 
population density in these months. By con- 
trast, the low numbers found at the end of 
autumn were probably due to migration to 
the undersampled marsh bottom. The de- 
crease after the breeding season was prob- 
ably due to mortality of the new-born snails. 
According to Taylor's law, the spatial distri- 
bution of V. contectus was contagious, and 
this behaviour, as Bovbjerg (1965), Duch 
(1976) and Brown (1979) have demonstrated, 
is characteristic of freshwater snails that tend 



50 



ELEUTHERIADIS & LAZARIDOU-DIMITRIADOU 



to aggregate on filamentous algae and large 
diatom clusters. Bithynia graeca in Lake Ker- 
kini also shows a contagious distribution 
(Eleutheriadis & Lazaridou-Dimitriadou, sub- 
mitted). Growth of V. contectus stopped at 
the end of autumn and in winter for about 4 
months. Growth pauses have also been re- 
ported for V. georgianas by Jokinen et al. 
(1982) and Buckley (1986) in New York. In 
contrast, Young (1975) for V. viviparus in En- 
gland, Bernardi et al. (1976) for V. ater in Italy, 
and Browne (1978) for V. georgianas in the 
USA noted that growth was continuous 
throughout the year, although growth rate 
varied seasonally. Rapid growth during 
spring may be due to the favourable water 
temperatures (Fig. 2) and oxygen concentra- 
tions (Fig. 3) that prevailed during this period 
in the Strymonas marshes. Water level and 
water temperature seem to influence the on- 
set of birth. Fully developed young were 
found throughout the year in the brood sacs 
of the adult females, so it appears that adult 
snails choose the most favourable environ- 
mental conditions for the release of young 
snails. The fact that both internal changes in 
this species concerning the maturation of the 
gonads correspond to external morphomet- 
ric changes in the shell agrees with results 
reported for other prosobranch species of 
the family Littorinidae (Daguzan, 1975), for 
Monodonta lineata (Daguzan, 1991), and for 
8. graeca (Eleutheriadis & Lazaridou-Dimitri- 
adou, submitted). Viviparus is a genus show- 
ing considerable variation in the duration of 
life. Viviparus contectus has a multiyear life 
cycle, and there are some differences in the 
pattern of the cycle within the genus. Such 
European investigators as Samochwalenco & 
Stanczykwoska (1972) reported that V. con- 
tectus and V. viviparus lives up to 4 years; 
Young (1975) reported that V. viviparus lives 
up to 2 years, and Ribi & Gebhardt (1986) 
reported that V. ater lives 5 to 8 years. A Ca- 
nadian population of V. malleatus was re- 
ported to live for 5 years (Stanczykwoska et 
al., 1971). In the USA, populations of V. geor- 
gianus were reported to have a 2 to 3 year 
life-span (Van Cleave & Lederer, from Vail, 
1978; Browne, 1978; Jokinen et al., 1982) 
and 4 years (Buckley, 1986). These studies 
indicate that Viviparus life span may be a trait 
determined by habitat factors. The compari- 
sons in production among freshwater snails 
were done by use the turnover times, be- 
cause productivity rates are very sensitive to 
difficulties of assessing environmental space 



in calculating densities for biomass (Russell- 
Hunter & Buckley, 1983). The turnover time 
for V. contectus is short and reflects relatively 
high levels of productivity. The value of 1 13.7 
days is low compared with values from other 
freshwater prosobranchs. For four popula- 
tions of V. georgianus, the turnover time was 
477, 510, 393 and 421 days (Browne, 1978), 
for Bitliynia tentaculata 337 and 314 days for 
females and males respectively (Tashiro, 
from Russell-Hunter & Buckley, 1983), and 
for three population of Leptoxis carinata 372, 
311 and 303 days (Aldridge, 1982). All these 
populations are at least biennial. Low values 
were reported by Lévêque (1973) in Lake 
Chad for three annual prosobranchs snails 
including 74.5-117 days for Melanoides tu- 
berculata, 101-126 days for Cleopatra buli- 
moides, 56-70.2 days for Bellamya unicolor, 
and in Lake Kerkini 77.9 days for an annual 
population of B. graeca (Eleutheriadis & 
Lazaridou-Dimitriadou, submitted). The dif- 
ference in turnover time of V. contectus com- 
pared to other biennial and triennial popula- 
tions must be due to lack of competition with 
other freshwater snails; in two years' study, 
only small numbers of Valvata piscinalis and 
Lymnaea stagnalis were recorded. There is 
also little direct human intervention on these 
marshes. 

Viviparus contectus, being an A-strategist, 
seems to be able to profit the favourable con- 
ditions even when the climate shows a sud- 
den difference and its parameters do not 
follow the characteristic cycle of the Mediter- 
ranean climate at the marshes of Strymonas 
River. 



ACKNOWLEDGEMENTS 

We would like to thank Dr. G. Dussart from 
Canterbury Christ Church College for his 
comments on an earlier draft of this paper and 
the two anonymous referees of this journal. 



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Revised ms accepted 28 Nov 1994 



MALACOLOGIA, 1995, 37(1): 53-68 

COMPARATIVE LIFE CYCLE AND GROWTH OF TWO FRESHWATER 

GASTROPOD SPECIES, PLANORBARIUS CORNEUS (L.) 

AND PLANORBIS PLANORBIS (L.). 

Katerine Costil & Jacques Daguzan 

Laboratoire de Zoologie et Ecophysiologie (L. A. INRA & URA 1853), Université de Rennes I, 
Campus de Beaulieu, Av. du Général Leclerc, 35042 Rennes Cedex, France 

ABSTRACT 

The shell growth and life cycle of two natural populations of Planorbarius corneus and 
Planorbis planorbis were studied for 16 and 17 months, respectively. These planorbid popu- 
lations lived in ponds where they exibited great annual density variations, which could be 
related to environmental conditions, snail behaviour and, especially, their life cycle. The pop- 
ulation of Planorbis planorbis showed a life cycle with two breeding periods per year, and 
consequently, two generations. Whereas both generations were semelparous and lived for 1 1 
months, they grew with different seasonal patterns. But of the two species, Planorbarius cor- 
neus growth seemed more influenced by the climate. For the population of this species, an 
annual life cycle with two generations was observed in 1987, whereas only one spring gener- 
ation seemed to be present in 1986 and 1988. In 1987, the vernal generation, showing an 
estimated maximum life span of 18-20.5 months, was potentially iteroparous, and the estival- 
autumnal generation living 15-21 months was basically semelparous. Life-cycle variations of 
natural populations of freshwater snails are reviewed. 
Key words: shell growth rate, life cycle, Planorbidae, population dynamics, reproduction. 



INTRODUCTION 

Life cycles of freshwater snails are of the 
highest importance for the study of their bi- 
ology because they can be viewed as a syn- 
thesis of the main life-history traits of snail 
populations. Such studies have been per- 
formed for planorbid temperate species (Rus- 
sell-Hunter, 1961; Boerger, 1975; Young, 
1975; Eversole, 1978; Alfaro Tejera, 1982; 
Lodge & Kelly, 1985; Byrne et al., 1989; Ca- 
quet, 1993). Planorbis planorbis has been re- 
ported to show an annual life cycle (De Coster 
& Persoone, 1970; Dussart, 1979), whereas 
the life cycle of P. corneus is almost unknown. 
In England, a population of P. corneus was 
studied for only four months (Berrie, 1963). 
Moreover, freshwater snails present great in- 
traspecific variation in life-history patterns 
(Calow, 1978; Brown, 1985), and this plastic- 
ity has been considered to be of fundamental 
selective value in their evolution. (Russell- 
Hunter, 1961). An observed life history is the 
result of both long-term evolutionary forces, 
and the more immediate responses of an or- 
ganism to the environment in which it is and 
has been living (Begon et al., 1990). 

The present data constitute part of a set of 
results on the biology and the ecology of Ar- 



morican freshwater gastropods (Costil, 1993, 
1 994; Costil & Daguzan, 1 994). The aim of the 
present study was to determine the life cy- 
cles of the populations of P. corneus and P. 
planorbis in order to compare them with life- 
history strategies of other freshwater snail 
populations. Special attention was given to 
snail shell growth. 

MATERIAL AND METHODS 
Study Sites 

The population of P. corneus was studied 
for 17 months in pond Le Boulet, located 35 
km north of Rennes, east Brittany (48-'20'N, 
1''38'\/V). The population of P. planorbis living 
in pond La Musse, 35 km southeast of 
Rennes (48'"00'N, 1°58'W), was sampled for 
16 months. These continuous studies were 
preceded and followed by instantaneous ob- 
servations made in 1986 and in 1989. 

The sampling areas in the large ponds (Le 
Boulet: 120 ha.; La Musse: 49 ha.) were the 
shallowest (depth of 20-50 cm) and the most 
eutrophic parts. Vegetation contained nu- 
merous aquatic and amphibious macro- 
phytes (Clement, 1986; Costil, 1993), and the 
bottom was covered by mud. Table 1 sum- 
marizes the results of water chemical analy- 



53 



54 



COSTIL & DAGUZAN 



TABLE 1. Water chemistry in the two study ponds; the unit is mg/l except for conductivity (|.iS/cm) and 
pH (pH unit); S.M. = matter in suspension; the analyses were performed in May 1988. 





S.M. 


CON 


Ca2* 


Mg2- 


pH 


Total iron 


Total 
mangenese 


Le Boulet 
La Musse 


80 
150 


160 
160 


13.8 
12.6 


6.0 
4.3 


7.3 
8.7 


3.17 
1.05 


1.4 

1.3 




N-NO3 


N-NO2 

10^2 


N-NH/ 
10 2 


Total 
nitrogen 


P-PO/ 
10-2 


Total 
phosphorus 




Le Boulet 
La Musse 


1.53 
0.39 


1.4 
1.3 


9.0 
8.0 


2.11 
1.86 


2.1 
0.9 


5.6 10 2 
2.4 10 2 





ses. Because of human interferences, the 
water level was subject to great variations (up 
to ± 180 cm at the study site in La Musse). 
Planorbarius corneus lived with 10 coexisting 
gastropod species (4 planorbids, 3 lym- 
naeids, 1 physid and 2 prosobranchs), 
whereas P. planorbis shared its habitat with 7 
species (3 planorbids, 3 iymnaeids and 1 
physid). In both ponds, birds and fishes that 
include molluscs in their diets were present, 
e.g. Anas platyrhynchos L. and Aythya 
fuligula L., Rutilus rutilus L. and Abramis 
brama L. 

Sampling 

Samples were taken fortnightly from May 
5, 1987, to October 18, 1988, for P. corneus, 
and from April 14, 1987, to August 16, 1988, 
for P. planorbis. Sampling was sometimes 
impossible because of ice cover or flooding. 
Random sampling took place in a limited 
zone of 50 m^ surface. In mid September 
1987 in pond La Musse, the deterioration of 
the environment leading to the disappear- 
ance of the studied population obliged us to 
transfer the study site from the south to the 
north bank, a few meters away. The snails, 
however, from both banks belonged to the 
same population. 

The snails were collected using a pond net 
(1 mm mesh) and a wood frame delimiting a 
sampling surface of one square meter. This 
sampling method was chosen especially be- 
cause it respects the environment and allows 
long-term study. On every sampling date, we 
tried to collect at least 100 individuals. The 
number of sampled m^ depended on the 
snail density and environmental conditions, 
and fluctuated from 3 to 10 for P. planorbis, 
and from 3 to 15 for P. corneus. The number 
of collected snails sometimes reached 380 
(P. planorbis) and 389 (P. corneus), but sam- 



pling difficulties (particularly ice cover or 
flooding) did not always allow us to collect 
1 00 snails. In the field, living snails and empty 
shells were counted (per m^), and measured 
(maximum shell diameter) using a vernier cal- 
liper (to the nearest of 0.05 mm). The snails 
were then returned to the study site, while the 
empty shells were removed. Egg capsules 
were sampled to determine periods of repro- 
duction. 

Sample Treatment 

The results were recored in 1-mm size 
classes. The number of individuals in each 
size class was expressed as a percentage of 
total number, establishing size-frequency 
histograms. The cohorts, represented by 
gaussian structures, were discriminated us- 
ing Bhattacharya's (1967) method. On every 
sampling date, a mean shell diameter (± stan- 
dard error) was calculated for each cohort. 
Each cohort was assumed to be representa- 
tive of one generation resulting from a spe- 
cific reproductive period. The empty shells 
were attributed to a particular cohort if pos- 
sible. 

The observed life span of a cohort corre- 
sponded to the time from recruitment until 
death. For the "real life span," we had to add 
the time necessary for the snails to reach the 
recruitment size. This time was known if the 
water temperature in the field and the growth 
results of the laboratory experiments were 
taken into consideration (Costil, 1994). 

Von Bertalanffy's model was used to de- 
scribe the growth of the vernal and estival or 
autumnal cohorts (Von Bertalanffy, 1938). It is 
given by the equation: 



Dt = D^3, [1-е 



K(t to)! 



where D, is the diameter at time t; D^ax' ^he 
asymptotic maximum diameter; K, a growth 



PLANORBID LIFE CYCLES 



55 



rate coefficient; tg, the hypothetical time 
when D is equal to "zero" (minus the duration 
of the egg stage). К and L^g^ are determined 
according to Ford-Walford's method by the 
slope and intercept on the x-axis of the re- 
gression line of growth rate on size, respec- 
tively. 



RESULTS 

Population Density 

The mean densities of P. corneus and P. 
planorbis were respectively 20.0 (S.E. = 3.5) 
and 37.8 (S.E. = 5.9) individuals/m^, but great 
annual variations were noted for both species 
(Fig. 1). The maximum density was the same 
(127 individuals/m^), but it was observed at 
different dates (P. planorbis: 07-07-87; P. 
corneus: 20-10-87). 

Life Cycle 

Two reproduction periods were found, a 
vernal for both species and an autumnal or 
estival-autumnal (16 weeks) for P. planorbis 
and P. corneus, respectively (Table 2). For P. 
planorbis, autumnal reproduction was only 
observed on two sampling dates. On Octo- 
ber 13, 1987, the site was inaccessible and 
perhaps egg capsules were present (repro- 
duction period for a minimum of two, possi- 
bly up to four weeks). 

The percentages of empty shells in relation 
to sampled live snails varied from 0.4 to 
26.8% for P. corneus, and from 0.0 to 32.4% 
for P. planorbis (Fig. 2). They were especially 
high in July 1987 for the first species, and in 
August 1987 and in April 1988 for the latter. 

For two consecutive years, the maximum 
shell diameter of the population of P. corneus 
was observed in May (20.9 mm on 19-05-87 
and 1 8.9 mm on 31 -05-88), whereas the min- 
imum (6.9 mm) was noted in March 1988. For 
P. planorbis, the minimum and maximum 
shell diameters were 4.2 mm (23-05-87) and 
11.8 mm (26-05-87), respectively. These 
changes in mean diameter of the population 
reflected the succession of cohorts that ap- 
peared, grew and died. Each cohort repre- 
sented a generation start after a particular 
reproductive period and descended from the 
same parent generation. 

At the beginning of the study, the popula- 
tion of P. corneus corresponded to cohort 
G1, the mean diameter of which was 18.9 



mm (Fig. 3). One month later, the diameter 
reached 23.7 mm and the snails reproduced. 
Some individuals of the cohort Gl lived until 
September 22, and some until mid Novem- 
ber. The very large shells (25-28 mm) were 
thicker and more eroded than the large shells 
(22-23 mm). Cohort 02 appeared on June 2, 
1987, and the largest snails laid egg capsules 
in summer 1987. The individuals of 02 over- 
wintered and, after May, except for observa- 
tions made on September 20, 1988 (24 indi- 
viduals in a restricted area), the number of 
survivors was low. Cohort 03 appeared on 
August 25, 1987, continued to be alive until 
the end of the study. Individuals of 03, but 
also survivors of 02, which had laid egg cap- 
sules in previous summer, were the parents 
of cohort 04. This cohort, recruited on May 
31, seemed not to reproduce, although three 
small snails were collected on October 4, 
probably belonging to cohort 05. 

In the case of P. planorbis, the population 
showing a mean diameter of 8.6 mm on April 
14, 1987, was mainly made up of one cohort 
(01) (Fig. 3). This cohort coexisted with a 
more aged cohort (OO; mean size of 15.7 
mm), which was no longer found in the mid- 
dle of June. 01 retained a relatively large 
number of snails until June 9, when the first 
newly hatched snails of cohort 02 appeared. 
After ovipositing in autumn (mean diameter of 
8.2 mm), the individuals of 02 did not disap- 
pear, and a lot of them were collected on 
March 1 5. Snails of 03 were seen for the first 
time on October 27, 1987. However, consid- 
ering their relative large size and the period 
when egg capsules were observed, it 
seemed that recruitment had already oc- 
curred on October 13. (On this date, we 
could not sample because of flooding.) In 
spring 1988, individuals of 03 gave the co- 
hort 04. From July 5, 1988, the snails of co- 
hort 03 contributed less than ^0% to the to- 
tal population. 

For P. corneus, the observed life span of 
cohort 02 was 70 weeks (about 16 months). 
The number of these snails was sometimes 
very low or null on certain sampling dates. 
Moreover, the individuals of cohorts 01 and 
02 were very similar in size at the beginning 
of May for two consecutive years. So, 02 ap- 
peared to be homologous to 01, and its 
members could survive six weeks after Oc- 
tober 4, as was the case of 01 in 1987. The 
observed life span of 02 was estimated to be 
from 70 to 76 weeks. If the correction factor 
and the size of 02 on the recruitment date 



56 





180-, 




160- 


^-^ 




fVi 


140- 


h 




•v. 




_J2 


120- 


n 




с 






100- 


>^ 




4-) 




(Л 


80- 


С 




<и 




■о 


60- 


с 




о 




4-> 

га 


40- 


э 




п 




о 


20- 



COSTIL & DAGUZAN 

А 




1 — I — I I I — I — гп — I — I I I I I I I I 1 I I I Т I I I I I I I — \ — Г~1 — г~1 — г 

о — 10 — гО|— rjj— rilO rílO rJlO — 'lO —■I— rí|<M|0 CNll— 'jO — mi— ' íNi'— (N|tNjO fS.O --> 



8 9 10 1112 



1234 5 6789 10 

Study dates (days & months) 



(Л 

с 

О) 

т: 

с 
о 



э 
о. 
о 

Ol 



180 -| 
160- 
140- 



Е 



^ 120 

го 

с 

<л .^^ 
^ 100 



80- 



60- 



40- 



20- -^ 



В 




т — I — I — I — I — I — 1 — I — г 



I |— rtjö rii 1 



-т — I — I — I — Г 

■3- — «Л !^ Г^ О 
jOlO — Г)|Г1 |— 



1 — I — I — I — I — I — г 



-1 — I — I — I — г 

-• íTí а\ п ^ 
о rliC — 10 — 



)|0 rliC — |< 



78 9 1011121 3 4 5 б 7 8 

Study dates (days & months) 



FIG. 1. Changes in population density with time: Mean ± S.E.. A: Planorbahus corneus (from April 1987 to 
October 1988); B: Planorbis planorbis (from May 1987 to August 1988). 



were taken into consideration, the "real life 
span" was then from 79 to 85 weeks (18 to 
20.5 months). At the end of the study, the 



snails belonging to cohort G3 measured 24 
mm, that is, 2 mm lower than the maximum 
size noticed for G2. Their growth curve did 



PLANORBID LIFE CYCLES 



57 



30 П 




о -^lO -^ mi— <N|— rJiO oiiO r^iO — 40 —I— <Ч|га|0 cnJi— lO — roi-^ cni-^ rsiiHiO «NiO — 
5 6 7 8 9101112123 4 5 6789 10 

Study dates (days & months) 



40n 




■^ 00 <N ЧО On 
— fNI— rJlO 



Гг^Г~- — ^^-tncbr^OT^OOriON-^l/ICJvO-^^t^— '<r)0N(N40 



rJiO 



— -З" — m 

rilOIC — 



rilrJI— riiO <N|— 'lO —I— rii— ' riiO c-no —10 — 



JjO <N|— 'jO —I— rll 

4 5 6 78 910111213 4 5 678 

Study dates (days & months) 

FIG. 2. Variation of the number of collected empty shells in relation to the number of live snails collected. 
A: Planorbarius corneus; B: Planorbis planorbis. 



58 



COSTIL & DAGUZAN 



TABLE 2. Features of reproduction period (R. P.) in Planorbarius corneus and Planorbis planorbis] the 
water temperatures, recorded on every study date at midday, correspond to minimum and maximum 
values during the reproduction periods. 











Water 




Start of the 


End of the 


Duration 


temperature 




R.P. 


R.P. 


(weeks) 


(C) 


Planorbarius 


19-05-87 


16-06-87 


4 


16-20 


corneus 


28-07-87 


17-11-87 


16 


9.5-28 




17-05-88 


28-06-88 


6 


15-22 


Planorbis 


28-04-87 


23-06-87 


8 


12-22 


planorbis 


15-09-87 


29-09-87 
(13-10-87?) 


2 

(4?) 


14.5-18.5 




11-05-88 


19-07-88 


10 


15-29 



not show a plateau, typical of an asymptotic 
growth. Moreover, the individuals of G3 were 
not found in sannpies collected during spring 
1989. The observed life span was estimated 
to be from 60 to 80 weeks. The "real life 
span" varied then from 67 to 87 weeks (15 to 
21 months). 

For P. planorbis, the cohort 02 showed an 
observed life span of 44 weeks and a "real 
life span" of 48 weeks. The population study 
was stopped in mid-August 1988, when five 
individuals of 03 were collected. If we con- 
sider 03 as the homologue of 01, we could 
say that 03 lived until the beginning of Sep- 
tember 1988. So, the cohorts 02 and 03 had 
the same observed (44 weeks) and "real life 
span" (48 weeks or 11 months). 

Growth of the Vernal and 
Estival-Autumnal Cohorts 

In P. corneus, strongly different growth 
patterns were noted, as evidenced by the co- 
horts (Fig. 4). In the first sample, the mean 
diameter of individuals of cohort 02 was 6.4 
mm. After 6 weeks, it reached 53% of the 
maximum size, that is, 13.8 mm, and the 
maximum growth rate attained 2.1 mm/week 
(Fig. 5). A second peak (1.5 mm/week) was 
observed for planorbids one year old. On the 
other hand, from December 15 to April 19 
(age: 29-45 weeks), shell growth gain did not 
exceed 2.3% (rates below 0.035 mm/week). 
For the growth of 03 cohort in the field, two 
periods appeared to be particularly favour- 
able: at the time of cohort recruitment (rates 
higher than 1 .05 mm/week), and from April 
19 to mid-June (age: 29-45 weeks, mean 
rate of 1 .2 mm/week, and so the size 
changed from 13.6 to 20.1 mm). During the 
winter and in July and August, shell growth 
was slow or null. The mean growth rate was 



slightly higher for 03 than for 02 (0.35; S.E. = 
0.09 and 0.29; S.E. = 0.08). Nevertheless, in- 
dividuals of both cohorts reached a size of 
about 25 mm at the end of their life. 

The growth rate coefficient of Von Berta- 
lanffy's model (k) was equal to 0.046. For the 
entire population of P. corneus, the shell 
growth in terms of individual age was given 
by the relation: 

D, = 37.31 [1-е oo46(t.o.5)j. 
time unit of 14 days. 

The theoretical diameter for maximum age 
estimated in the field (32.4 for snails 20 
months old) was higher than maximum size 
observed in the field (28 mm) (Table 3). 

In the case of P. planorbis, the snails of 
cohort 02 reached 65% of their maximum 
size eight weeks after recruitment; maximum 
rates were of 0.85 and 0.80 mm/week (Figs. 
4, 6). Thirty-two weeks were necessary to at- 
tain 89% of their size before growth started 
again and the death of the cohort. For the 
cohort 03, a long recruitment period influ- 
encing the growth rates was observed. The 
snails reached the two-thirds of the maxi- 
mum size after 26 weeks, and two peaks 
(more than 0.7 mm/week) were noted in 
spring and in summer 1988. The mean 
growth rates of the cohorts 02 and 03 were 
0.21 (S.E. = 0.05) and 0.19 (S.E. = 0.05) mm/ 
week, respectively. 

The theoretical shell growth of the popula- 
tion in relation to snail age was given by the 
following relation: 

D, = 13.4 [1 - e °69(t.i.2)^. 
time unit of 14 days. 

According to Von Bertalanffy's model, the 
maximum mean diameters of 02 (11.3 mm) 
and 03 (1 1 .6 mm) conferred on these cohorts 
a life span of 11-12 months (Table 3). 




59 



mo\rí\00,'^oo, — mocrj400 mr^ — 1л rjvorn poo<o\ mr^— ■^oofsvom^o ■^00 

о — 10 — rr\\— rl — r) о rio rilO —10 —1— <N|H lO (Nl^lO — mi'-« C^t'^ <N| fSiO <N|0 — 



8 9 101112 12 34 5 6789 10 



5 6 

1987 



10 1112 12 3 4 
1988 

Study dates (days & months) 



Egg laying 



Diameter (mm) 




■^ — I — I — I — I — I — I — I — I — г 

Tfoo оофг^ r^_-rt- _ina\ r-o-^ ooo40\ -— >л (N\o — •^г;~' îCî'^îy^ 
— rii— гьог) |Cr»|0|0 — oílcJi—cMiOcNi— |0— I— (NI— cMiOrJ 10— lO — 



4 5 6 

1987 



7 8 



1011121 3 4 5 6 7 8 

1988 

Study dates (days & months) 



FIG. 3. Changes in mean shell diameter of Planorbarius corneus (A) and Planorbis planorbis (B) (± S.E.) with 
time (from May and April 1987 to October and August 1988, respectively), at the Le Boulet and La Musse 
ponds respectively. The numerals correspond to percentages denoting the contribution of each cohort to 
the total population. For P. corneus, Gl, G2 and G4 represent the spring generations, and G3 the estival- 
autumnal one. For P. planorbis, the spring generations are GO, G2 and G4, whereas the autumnal gener- 
ations are Gl and G3. 



60 



COSTIL & DAGUZAN 



100 
90 
80 
70 
60" 
50- 
40- 
30- 
20 
101 




Ф 
E 

"O 

E 

Э 

E 

X 

a 
E 

Ф 
Ф 
E 

5 Q-i 1 1 1 1 1 1 1 1 1 1 « 1 f 1 I 

° O 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75 

Observed age (weeks) 



Ф 

Ф 

E 
ja 

"O 

E 

Э 

E 

X 

со 
E 

Ф 
Ф 

E 

a 



100 
90 
80 
70 
60 
50 
40 
30 
20 
10 
O 




1 1 1 1 1 1 1 1 I 

5 10 15 20 25 30 35 40 45 

Observed age (weeks) 

FIG. 4. Relation between the snail age and the percentage of maximum diameter attained by the individuals 
belonging to the vernal (C2) and the estival or automnal (C3) cohorts. A: Planorbarius corneus; B: Planorbis 
planorbis. 



PU\NORBID LIFE CYCLES 



61 



Cohort G2 



temperature 



Growth rates 
(mm/wee k) 




-I 1 1 1 1 1 • ? • "I 

5 10 15 20 25 30 35 40 45 50 55 60 65 70 
Observed age (weeks) 



Cohort G3 



Water temperature 
(°C) 

-» V 



Growth 




Observed age (weeks) 

FIG. 5. Variation of the water temperature at Le Boulet pond, and clianges in growtin rates for the vernal (C2) 
and the automnal (C3) cohorts of Planorbarius corneus. Sp = spring; Su - summer; F - fall; W = winter. The 
value corresponding to C3 snails at the age of 13 weeks is put in brackets because it is an abnormal value 
due to sampling difficulties. 



62 



COSTIL & DAGUZAN 



TABLE 3. Theoretical relation between the age and the shell diameter (D) of Planorbahus corneus and 
Planorbis planorbis according to Von Bertalanffy's model, H = hatching. 



P. 

corneus 


Age (months) 
D (mm) 


H 

1.2 


1 
4.0 


3 
10.3 


6 

17.2 




12 
26.3 


18 
31.2 


20 
32.4 


P. 
planorbis 


Age (months) 
D (mm) 


H 
0.8 


1 
2.7 


3 
5.5 


6 

8.4 




10 
10.6 


12 

11.4 






DISCUSSION 






natelv 


' declines 


as 


the water level inc 


reases. 



Density Variations 

Variation in population structure appears to 
be a major factor explaining variation in snail 
density. In our study, the recruitment of newly 
hatched snails had a strong effect on the den- 
sity, whereas the cohort disappearance af- 
fected the density more or less progressively. 
We do not know exactly how long the resi- 
dence time of the empty shells in the studied 
ponds is and when the corresponding snails 
were dead. Such a topic has not been exam- 
ined much. Hunter (1990) has reported that 
adverse water chemistry (low pH and/or low 
calcium concentration) has a much greater 
effect on shell dissolution than does presence 
or absence of periostracum. Moreover, empty 
shells do not have an absolute value, because 
they could accumulate in certain areas. Nev- 
ertheless, the percentages of empty shells 
and above all their variation helped us to de- 
termine the life cycle of both populations, and 
to explain the variations in their density. For P. 
planorbis, great numbers of empty shells and 
low densities could be attributed to death of 
cohorts. In summer, the disappearance of G1 
and G3 took place, whereas in spring the dis- 
appearance of G2 occurred. On July 14 and 
28, 1987, the density of P. corneus was low 
and the percentage of empty shells high (20- 
27%). The reproductive effort of the largest 
individuals seemed to be responsible for their 
death, whereas the high mortality of small in- 
dividuals might be due to prédation. The pred- 
ators seem to be small invertebrates unable to 
eat whole shells, such as insects or leeches, 
because a lot of empty shells were pierced. 
Nevertheless, the major prédation on fresh- 
water snails is exerted by vertebrates (Lodge 
et al., 1987). According to Eisenberg (1966), 
the whole prédation could lead to the death of 
93% to 98% of the young Lymnaea elodes 
(Say). 

The snails were sampled using a pond net 
which respects the environment, but the ef- 
ficiency of this sampling method unfortu- 



Thls is especially illustrated in winter for P. 
corneus, and on June 7, 1 988, when the den- 
sity of P. planorbis population was less than 
6 snails/m^ at the flooded study site. On the 
other hand, during dry periods, snails could 
be seen on the mud and easily collected. Such 
was the case in March 1988 for P. planorbis 
and in September 1988 for P. corneus. Snail 
behaviour also influenced their density. When 
the environmental conditions became unfa- 
vourable in winter, we observed some indi- 
viduals of P. corneus sinking into substratum 
crevices or even into mud. It was then very 
difficult to collect them. Such behaviour has 
been reported for Lymnaea catascopium (Say) 
(Pinel Alloul, 1978). At the same time, some 
individuals of P. corneus were seen moving on 
the ice cover on December 1 and 15, 1987. 
Nevertheless, the extreme climatic conditions 
(cold and hot) appeared particularly unfavour- 
able for the population density of P. corneus. 
In summer, lack of dissolved oxygen into wa- 
ter was a problem, as was the case in late July 
1987, when chlorophytes pullulated at the 
study site and no individual of P. planorbis 
was sampled. Moreover, Eisenberg (1966) 
emphasized the importance of food for the 
regulation of density in a natural population of 
L. elodes. The death and then the regrowth of 
submerged macrophytes led to changes in 
the densities of those snails inhabiting them 
(Lodge et al., 1987). Lymnaea peregra and 
Valvata piscinalis (Mijller) exhibited low resis- 
tance to habitat disturbance (decline of sub- 
mersed macrophytes), but high adjustment 
following the disturbance. The maximum den- 
sity for P. corneus (127 snails/m^) was noted 
three days after a storm occurred in Brittany 
with winds of 140 km/h. The accumulation of 
individuals olAnisus rotundatus (Poiret) in lim- 
ited areas attributed to wind was also re- 
ported by Marazanof (1970). 

Life Cycle 

Different reproductive periods were deter- 
mined according to the cohort to which the 



PLANORBID LIFE CYCLES 

Cohort G2 



63 



Water temperature 



Growth rates 
(mm/week) 



Г 1.0 




15 20 25 30 35 40 45 
Observed age (weeks) 



Cohort G3 



temperature 



15 20 25 30 35 
Observed age (weeks) 



Growth rates 
(mm/week) 

Г 1,0 




FIG. 6. Variation of the water temperature at La Musse pond, and cinanges in growth rates for the vernal (C2) 
and the automnal (C3) cohorts of Planorbis planorbis. Sp = spring; Su = summer; F = fall; W = winter. 



64 



COSTIL & DAGUZAN 



majority of the parents belonged. In the stud- 
ied population of P. corneus, the egg-laying 
period began in May and ended in Novem- 
ber, but we accepted two periods. The esti- 
val-autumnal reproduction period lasted for 
1 6 weeks (the parents belonged to the cohort 
G2). However, at the end of this period, we 
could not exclude an egg-laying by the larg- 
est individuals of 03 estival cohort (13 mm on 
November 17, 1987). Moreover, no egg cap- 
sules were found in August or in October 
1987. Perhaps some were in the field, but it 
was very difficult to see them among the 
dense vegetation. The length of the egg-lay- 
ing period was due to the inter-individual 
growth variation. In L. catascopium, all the 
snails belonging to spring generation were 
not mature at the same time, and they con- 
tinued to reproduce as long as the water tem- 
perature allowed it (Pinel Alloul & Magnin, 
1979). According to Berrie (1963), the repro- 
duction period of P. corneus was short. On 
the other hand, De Coster & Persoone (1970) 
sampled very small P. corneus (0-2 mm) from 
April to September. Concerning P. planorbis, 
the spring reproduction periods were longer 
than the autumnal period. In northwest En- 
gland, P. planorbis also showed two egg-lay- 
ing periods, one in February and the other in 
July (Dussart, 1979). 

According to Precht (1936), P. corneus did 
not reproduce in autumn or in winter, and an 
endogenous rhythm had to be suggested, be- 
cause the snails brought in the laboratory at 
23'C did not lay eggs either. This author 
added that P. corneus began to reproduce 
when the temperature reached 12 'C. The 
minimum threshold temperature for the re- 
production of freshwater snails appears to be 
between 7' С and 12 С (Boerger, 1975; Dun- 
can, 1975; Eversole, 1978). Three egg cap- 
sules were laid by P. corneus reared at 8' С 
(De Wit, 1955). In our study, the reproduction 
period of both species began when temper- 
ature reached 1 5-1 6 0, which was above the 
minimum threshold. In spite of suitable tem- 
peratures, the genital organs could be imma- 
ture. Such a result was observed by Russell- 
Hunter (1961) in Gyraulus albus (Müller). 
Moreover, the freshwater snails could be 
more sensitive to temperature variations than 
to absolute temperatures. 

The main life-cycle patterns encountered in 
natural populations of freshwater snails have 
been described by Russell-Hunter (1961, 
1978) and reviewed by Calow (1978). During 
our study, P. planorbis showed a type as 
defined by Calow (1978), that is, an annual life 



cycle with reproduction periods occurring in 
spring and in autumn with parent generation 
replacement. The snails of the vernal cohort 
G2 did not survive until the next reproductive 
period. However, these individuals coexisted 
with the snails of the autumnal cohort for 28 
months. Both cohorts corresponding to two 
generations were semelparous, and their life 
span was estimated at 1 1 months. A life span 
of 1 2-1 3 months and an annual life cycle have 
been reported respectively by De Coster & 
Persoone (1970) and Dussart (1979). How- 
ever, the second author described a life cycle 
with egg-laying pehods completely brought 
forward in comparison with our results (re- 
cruitment of newly hatched snails in February 
and July instead of early May and September). 
Such an annual life cycle with two generations 
per year occurred in the following species: 
Lymnaea peregra (Müller) (Russell-Hunter, 
1961; Lambert, 1990), Lymnaea palustris 
(Müller) (Hunter, 1975), Physa fontinalis (L.) 
(De Wit, 1955; Russell-Hunter, 1961), Heli- 
soma trivolvis (Say) (Eversole, 1978); Bathy- 
omphalus contortus (L.) (De Coster & Per- 
soone, ^970), Armiger crista (L.) (Alfaro Tejera, 
1982), and A. rotundatus (Marazanof, 1970). 
For the latter planorbid species. Caquet 
(1 993) observed a semelparous life cycle with 
a maximum life span apparently reaching 
17-18 months. 

From a four-month study, an annual life cy- 
cle was attributed to P. corneus (Berrie, 1 963). 
According to different authors, the life span of 
this species in the field was 13 months 
(Hilbert, 1911), 2 or 3 years (Boycott, 1936; 
Boettger, 1944), and 4 years (Frömming, 
1956). Russell-Hunter (1978) has reported 
that biennal life-cycle patterns involve such 
larger pulmonates as P. corneus and Lym- 
naea stagnalis (L.) in higher latitudes or more 
oligotrophic waters (i.e., poorer temperature 
or trophic conditions). Like for P. planorbis, 
the life cycle of P. corneus in 1 987 was annual 
showing two generations. The estival-autum- 
nal generation was not replaced by the new 
generation (type B). So, other differences 
were also observed between the two species: 
longer life span of both generations and an 
annual life cycle close to a biennial (18-20.5 
months for G2; 15-21 months for 03, these 
life spans could be very similar); a longer sec- 
ond reproductive period; a spring cohort 
probably iteroparous to a certain extent and 
an estival-autumnal cohort probably semel- 
parous (the second egg laying period proba- 
bly missing in 1986 and 1988). At the begin- 
ning of May 1987, only one cohort was 



PLANORBID LIFE CYCLES 



65 



observed (G1). Its mean diameter was the 
homologous of the spring cohort G2 diame- 
ter at the same date in 1 988. In autumn 1 988, 
no egg capsule was present at the sampling 
site, although three small snails were col- 
lected on October 4 (mean diameter of 6.1 
mm). The second reproduction period might 
occur every other year or might be far less 
predictable, depending on annual climatic 
variations. In the pond Le Boulet in 1988, the 
water temperature was apparently not as 
high as in 1987, and shell growth was slower 
than in 1987. The climatic hypothesis was put 
forward by Vincent & Harvey (1 985) to explain 
both types of life cycle (short and long) en- 
countered in a Canadian population of Bithyn- 
ia tentaculata (L.). The number of genera- 
tions per year can also be related to the 
length of dry periods (Duncan, 1959; Ma- 
razanof, 1970). Lymnaea catascopium exhib- 
ited an annual life cycle with one generation 
in hard or medium waters, and two genera- 
tions in soft waters (Pinel Alloul, 1978). In L. 
peregra, snails from the exposed habitats 
matured earlier and put more effort into it 
than snails from the sheltered habitats; these 
differences in growth and reproduction could 
be explained in terms of differences in selec- 
tion pressure between habitats of varying 
exposure (Calow, 1981). Individuals of H. 
trivolvis from the eutrophic sites grew faster 
and exhibited an annual life cycle, whereas 
those from the mesotrophic site grew slowly 
and lived about two years, breeding in both 
summers (Eversole, 1978). From reciprocal 
transfer experiments. Brown et al. (1985) 
concluded: "genetic divergence among pop- 
ulations of L. elodes explained a compara- 
tively small proportion of the variation in life 
histories in comparison with proximal factors 
like habitat productivity. Nevertheless, snails 
from the vernal pond always grew more 
slowly, matured at a smaller shell length, and 
had higher fecundities than other popula- 
tions. These smaller differences may still be 
important over evolutionary time scales." 
These examples show that life-cycle varia- 
tions can be adaptative. The adaptative plas- 
ticity allows the populations to have maxi- 
mum productivity in given conditions and 
then to compensate for bad years (Huben- 
dick, 1958; Russell-Hunter, 1961). 



Snail Growth 

The shell growth of freshwater pulmonales 
is continuous until death (indeterminate 



growth). For both studied species, the growth 
differed according to time when a cohort had 
been recruited. The shell growth did not only 
depend on age of the animals, but the ob- 
served differences could be due to various 
physiological potentialities that remain to be 
studied. For ß. tentaculata, growth rates fluc- 
tuated from 0.17 mm/week to 0.80 mm/week 
with the seasonal trophic conditions (Pinel 
Alloul & Magnin, 1971). In L. peregra and L 
palustris, the vast majority of the interpopu- 
lation variation of shell growth rate appeared 
to result from non-genetic ecophenotypic en- 
vironmental influences and in particular from 
habitat productivity (Byrne et al., 1989). Cli- 
mate seemed very important for growth, es- 
pecially in the case of P. corneus. 

Spring is very favourable to the shell 
growth of P. corneus and other species (Ma- 
razanof, 1970; Pinel Alloul, 1978). In June 
1987, a marking experiment (with painting) 
allowed us to observe that some shells had 
grown from 0.75 of whorl to 1 .75 whorls in 
two weeks (diameters attaining respectively 
10.1 and 18.1 mm). In spring, theshell growth 
of young Lymnaea humilis (Say) was very fast 
reaching 7% per day (MacCraw, 1961). Dur- 
ing autumn, the studied snails grew with in- 
termediate rates. In summer (July-August) 
and in winter (December to March), a lower 
rate of shell growth was noticed for L. pere- 
gra (Lambert, 1990) and P. corneus inhabit- 
ing Le Boulet pond. In summer, the high tem- 
peratures (up to 26' 'C) monitored probably 
exceeded the optimum, which was close to 
20° С for the growth of the two studied spe- 
cies reared in the laboratory (Costil, 1994). 
For a population of P. corneus in England, 
Berrie (1963) recorded a mean size increase 
of 4% between July and August, and in- 
creases of 70% and 33% respectively be- 
tween June-July and August-September. In 
our study, the growth of individuals belong- 
ing to cohort G2 slowed down at the same 
period that the snails reproduced. Concern- 
ing the homologous cohort G4, no summer 
reproduction period was observed in 1988, 
but growth did not slow down. These facts 
about the cohorts G2 and G4 suggested the 
energy allocation theory which, on the other 
hand, was not confirmed by the cohort G3 
(growth slowed down after reproduction pe- 
riod). A slow or null shell growth during winter 
has been reported for many freshwater snails 
(Russell-Hunter, 1961; Calow, 1973; Vincent 
et al., 1981). Individuals of ß. contortus sam- 
pled in winter and then brought to the labo- 
ratory grew fast again (Calow, 1973). Natural 



66 



COSTIL & DAGUZAN 



population of aquatic molluscs can exhibit 
degrowth (decrease in unit mass of structural 
proteins through time) (Russell-Hunter, 
1985); according to this author, degrowth 
can be associated with reproductive or sea- 
sonal stress, an example being the overwin- 
ter starved individuals of P. corneus, which 
lost 44% of their tissue biomass over 126 
days (with 33% mortality). For the same spe- 
cies, Emerson (1967) has reported similar 
losses: 62.3% with 56% mortality after 58 
days of starvation; at this time, 95% of the 
original polysaccharides, 49% of the proteins 
and 22% of the lipids were metabolized. A 
very omnivorous diet could be responsible 
for the winter shell growth observed in P. plan- 
orbis and also L peregra (Russell-Hunter, 
1961), Physa integra and P. gyrina (Clampitt, 
1970). In the diets of both P. corneus and 
Planorbis carinatus (Müller) (close to P. plan- 
orbis), detritus formed over 85% of the food 
ingested and sand grains about ^0% (Reav- 
ell, 1980). In comparison with P. corneus, P. 
planorbis seemed far less affected by the cli- 
matic variations. The spring cohorts (G2 and 
G4) grew the fastest in July and August. Their 
renewal of growth at the end of life could be 
due to the late death of the largest individu- 
als. 

According to Von Bertalanffy's model, the 
largest individuals of P. corneus in the field 
were 14 months old. However, this model 
does not take into account the environmental 
conditions and their variations. It appears 
more suitable for P. planorbis than for P. cor- 
neus. The first species showed higher growth 
constant (k = 0.069) than the second (k = 
0.046), which illustrates a faster develop- 
ment. For comparison with other freshwater 
snails, some values of к are given (same time 
unit: 14 days): 0.024 for A. crista (Alfaro Te- 
jera, 1982), 0.057 to 0.485 for snails from 
Lake Tchad (Lévêque, 1971), 0.095 for L. per- 
egra (Lambert, 1990). 

The maximum size reached by animals in- 
habiting in a given site depends on many fac- 
tors, such as environmental conditions, but 
also genetic makeup and parasitic infection. 
Before death, the cohorts Gl and G2 of P. 
corneus respectively measured 27.4 or 25.9 
mm, and the size of the largest individuals 
reached 28 mm. These sizes were lower than 
the value that is usually given for this species 
(35 mm). According to the cohorts of P. plan- 
orbis, the mean diameter attained before 
disappearance fluctuated from 11.3 to 14.3 
mm. The maximum diameter recorded was 



16.1 mm, whereas the maximum size re- 
ported for this species is 20 mm. It is difficult 
to know to what extent the environment con- 
ditions influence the maximum size of the 
snails of a given species. In both ponds, the 
water mineralization was rather low, and 
flooding and drying occurred quite often, 
making the environment unstable. According 
to Byrne et al. (1989), the extended adult sur- 
vival and oviposition was a life-history trait 
that allows L. palustris to survive in marginal, 
unstable habitats. Such an observation could 
be made for P. corneus showing a potentially 
itereparous cohort and a very long annual life 
cycle, but not for P. planorbis. Nevertheless, 
for both species the spring cohort growth 
was rapid enough to allow a second repro- 
duction period per year (every year in the P. 
planorbis population and in 1987 for P. cor- 
neus). Moreover, the trophic conditions in 
both studied ponds appeared favourable for 
the coexistence of a great number of gastro- 
pod species. The environmental factors are 
of the highest importance in the life-history 
strategies of the freshwater snails. The great 
range of strategies used by these snails in- 
habiting various types of environment make 
them particularly useful for studies about ev- 
olutionary biology. 



ACKNOWLEDGMENTS 

We are grateful to Maria Lazaridou-Dimitri- 
adou for her comments on early draft of this 
manuscript. We also thank Stacy Payne for 
checking the english and Jean Luc Foulon for 
technical help. 



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Revised Ms. accepted 15 December 1994 



MALACOLOGIA, 1995, 37(1): 69-110 

WHEN SHELLS DO NOT TELL: 145 MILLION YEARS OF EVOLUTION IN 

NORTH AMERICA'S POLYGYRID LAND SNAILS, WITH A REVISION 

AND CONSERVATION PRIORITIES 

Kenneth С Emberton 

Department of Malacology, Academy of Natural Sciences of Philadelphia, 1900 Benjamin 
Franklin Parkway, Philadelphia, Pennsylvania 19103-1195 U.S.A. 

ABSTRACT 

A phylogenetic hypothesis for the 274 known polygyrid species is presented, based on 115 
anatomical, behavioral, and shell characters (39 of which are newly discovered or newly as- 
sessed), as corroborated in part by published allozyme data. The hypothesis differs little from 
that of Emberton (1994a), except for greatly increased resolution in the tribes Stenotremini and 
Polygyrini. A corresponding revision is presented that assigns species to 50 subgenera, 24 
genera, seven tribes, three infrafamilies, and two subfamilies. All taxa in the revision, as well as 
unnamed clades, are defined phylogenetically by shared derived characters. Nine new subge- 
neric names are introduced: Neohelix (Asamiorbis), N. (Solemorbis), Triodopsis (Brooksorbis), 
T. (Pilsbryorbis), T. (Macmillanorbis), T. (Vagvolgyorbis). Stenotrema (Archerelix), S. (Pils- 
brelix), and Millerelix (Prattelix). 

A separate phylogenetic analysis of polygyrid subgenera was conducted based on shell 
morphology alone, using 71 character states in 14 characters, all new or newly assessed, 
including ontogenetic characters scored from shell x-rays. The resulting shell-based hypothesis 
had only one-fourth the phylogenetic resolution of, and showed major topological discrepan- 
cies from, the anatomy-behavior-shell hypothesis. Thus, at present level of knowledge, poly- 
gyrid shells are inadequate for reconstructing phylogenetic history, and identifications of pre- 
Miocene fossils should be considered dubious at best. Remaining to be evaluated, however, 
are shell-surface microsculptures and ultrastructural layers. 

Museum and field surveys discovered the closest known polygyrid convergences in sympa- 
try on flat, umbilicate, and tridentate shell forms: Patera laevior and Xolotrema fasten at Hawes- 
ville, Harlan County, Kentucky; Appalachina sayana and Allogona profunda on Pine Moun- 
tain, Hancock County, Kentucky; and Inflectarius inflectus and Triodopsis fallax in Vinton 
County, Ohio. These provide starting points for analyses of naturally replicated experiments 
in evolutionary morphology, such as those already conducted on the globose shell form 
{Mesodon normalis and Neohelix major at numerous sites in the Southern Appalachian Moun- 
tains). 

Adult Triodopsis tridentata from which apertural barriers had been removed lost water 
27% faster than controls when retracted, and 9% faster when extended. Controls were 83% 
more successful than barrierless snails in forming epiphragms. Epiphragms reduced the rate 
of water loss by 3% in controls and by 38% in barrierless snails. Ramsay's (1935) hypothesis 
is extended to suggest that barriers and epiphragms slow evaporation not directly, but indi- 
rectly by interrupting natural convection currents between the aperture and the retracted snail's 
body. Because T tridentata and other triodopsins have larger barriers in more humid climates, 
barriers should also serve at least one other function, such as impeding invertebrate predators. 
A new hypothesis is proposed for the function of extremely obstructed shell apertures: to 
exclude water, allowing the snails to float to safety during floods. Polygyrids have many con- 
vergences on apertural obstruction by barriers, some extreme examples of which are illustrated 
together. 

Based on the phylogenetic hypothesis/revision, the most urgent remaining targets for 
polygyrid conservation are (1) Colombia's Isla de Providencia, where deforestation threatens 
the ancient, relic, uniquely live-bearing, endemic Giffordius; and (2) the northern coves of Pine 
Mountain, Harlan County, Kentucky, which harbor North America's most diverse land-snail 
communities, including four simultaneous cases of polygyrid convergence in sympatry. 

Key words: cladistics, phylogenetic taxonomy, shell ontogeny, paleontology, fossils, con- 
vergence in sympatry, functional morphology. Gastropoda, Pulmonata, Stylommatophora. 



69 



70 



EMBERTON 



INTRODUCTION 

The Polygyridae are an endemic North 
American family of land snails that are remark- 
able for their shell convergences in sympatry 
(due to iterative, punctuated evolution cou- 
pled with phenotypic and genetic, adaptive 
parallel environmental responses); their 145- 
million-year biogeographic history (paralleling 
that of, for example, plethodontid salaman- 
ders); and their evolution of hermaphroditic, 
external sperm exchange via several behav- 
iorally bizarre intermediates that remain ex- 
tant (Pilsbn/, 1 940; Webb, 1 974; Solem, 1 976; 
Emberton, 1981, 1988a, 1991a,b 1994a,b, 
1995a,b; Asami, 1988, 1993). Polygyrids cur- 
rently comprise 271 nominal and three unde- 
scribed species (see below), with a maximum 
sympatric diversity of ten species reported 
from Pine Mountain, Harlan County, Ken- 
tucky, U.S.A. (Hubricht, unpublished; Ember- 
ton, 1 995c), with many more species yet to be 
described and discovered in Mexico and Cen- 
tral America (F. Thompson, pers. commun.), 
and probably with some undiscovered spe- 
cies remaining in the Pacific Northwest (T. 
Frest, pers. commun.). Phylogenetic hypoth- 
eses for the family as a whole (Webb, 1974; 
Pratt, 1979; Emberton, 1994a) have been to 
genus only, and the most recent hypothesis 
omitted shell characters completely and had 
major unresolved polytomies. 

Polygyhd fossil shells of the Pleistocene 
and Pliocene are nearly all identical with 
Recent species (Hubricht, 1985, and pers. 
commun.; Emberton & Bogan, unpublished). 
Miocene and later fossils are generally as- 
signable to genus (Pilsbry, 1940; Auffenberg 
& Porten, 1992; Roth & Emberton, 1994). Ear- 
lier polygyrid fossils, however, which are rare 
but presumably valuable in reconstructing 
the first 125 million years of polygyrid history, 
could be difficult to identify because of multi- 
convergent, punctuated-equilibrium evolu- 
tion (Emberton, 1994a). One way of testing 
the value of early fossils is to make an hon- 
est, concerted attempt to reconstruct poly- 
gyrid phylogeny based on Recent shells 
alone. This has not previously been at- 
tempted. One possible source of new and 
useful characters for such an analysis — and 
for fossil identification — is shell ontogeny as 
viewed in x-rays (Ramirez, 1993). For exam- 
ple, a recent study discovered, using x-rays, 
a significant difference in whorl-expansion 
rate between the polygyrid tribes Triodopsini 
and Mesodontini (Emberton, 1994a). Thus a 



more general x-ray survey of polygyrid shell 
ontogeny could be productive. 

Non-mimetic sympatric convergences are 
important as naturally replicated experiments 
in evolutionary morphology (Emberton, 
1995a). Polygyrid non-mimetic convergences 
in sympatry fall into four distinct shell forms 
(Pilsbry, 1940) that have been called globose, 
flat, tridentate, and umbilicate shell-static 
clades (Fig. 1; Emberton, 1991b, 1994a). The 
globose clades show the closest conver- 
gences in sympatry (Solem, 1976; Emberton, 
1 981 ; Asami, 1 988, 1 993), of which the most 
extreme is between Neohellx major and Me- 
sodon normalis. Recent analyses of these two 
species have yielded important new insights 
into the ecological, genetic, and natural- 
selective influences on shell morphology 
(Emberton, 1994b, 1995a). The most extreme 
cases of sympatric convergence on flat, tri- 
dentate, and umbilicate shell forms have not 
been analyzed or even reported, however. 

Polygyrid shell evolution is further note- 
worthy for its convergences in extreme aper- 
tural obstruction by denticles and other shell 
structures (Fig. 2; Pilsbry, 1940; Zilch, 1959- 
60). Such apertural barriers appear in many 
forms among numerous land-snail clades 
(Zilch, 1959-60). Four hypotheses have been 
proposed concerning the function of these 
barriers: (1) to deter attacks by predatory in- 
sects (Cook, 1895; Boettger, 1921, 1935; 
Solem, 1972, 1974; Falkner, 1984); (2) to re- 
tard evaporative water loss (Boettger, as 
cited by Goodfriend, 1986; Rees, 1964; Paul, 
1974; Christelow, 1992); (3) to strengthen the 
aperture against accidental breakage (Paul, 
1974); and (4) to orient the shell during crawl- 
ing (Paul, 1974). A fifth hypothesis, proposed 
here for the first time, is suggested by some 
polygyrid cases of extreme apertural ob- 
struction existing in flood-prone environ- 
ments (Hubricht, 1985; Emberton, 1986): that 
some barriers function (5) to trap air within 
the submerged shell, preventing drowning 
and enhancing gene flow by allowing the 
snail to float downstream. None of these hy- 
potheses has been adequately tested using 
living snails (Goodfriend, 1986; pers. ob- 
serv.). 

Also untested is the likely hypothesis that 
some barriers perform two or more functions 
simultaneously. In the polygyrid tribe Triod- 
opsini, there is a correlation in several lin- 
eages — including that of the common spe- 
cies Thodopsis tridentata — between greater 
apertural obstruction and increased environ- 



POLYGYRID SHELL EVOLUTION 



71 




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72 



EMBERTON 




FIG. 2. Convergent shell-apertural obstruction among various polygyria subgenera. Species are (left to 
right, top row): Triodopsis (Haroldorbis) henhettae (ANSP 109734), Trilobopsis roperi (150631), Ashmunella 
mudgii (319743), Stenotrema (Stenotrema) unciferum (171138), Stenotrema (Stenotrema) maxillifer 
(170141); (bottom row): Millerelix (Millerelix) tamaulipasensis (317942), Millerelix (Prattelix) plicata (143448), 
Daedalochila (Upsilodon) hippocrepis (84629), Daedalochila (Daedalochila) uvulifera (10990), Inflectarius 
(Inflectarius) rugeli (1 16893). 



mental moisture (Vagvolgyi, 1966; Emberton, 
1988a). This implies that if apertural barriers 
retard evaporative water loss in T. thdentata, 
then they should also serve at least one ad- 
ditional function, such as deterring predators 
or trapping air. 

Polygyrid conservation is relatively ad- 
vanced, with at least five rare taxa currently 
listed as endangered or threatened: Patera 
clarki nantahalae, Fumonelix arc hen, F. or- 
estes, F. jonesianus, and Triodopsis playsay- 
oides. Thanks to this recognition, these taxa 
are receiving the protection they need to sur- 
vive. Phylogenetic analysis, however, can 
provide insights into conservation priorities 
beyond the rarity of individual taxa. Polygyrid 
conservation has never been considered in a 
phylogenetic context. 

The purposes of this paper are (1) to con- 
duct a phylogenetic analysis of the Polygy- 
ridae to the species-group/subgeneric level; 
to use the resulting phylogenetic hypothesis 
(2) to taxonomically revise the family; (3) to 
conduct an independent phylogenetic analy- 
sis based on shells alone, incorporating 
x-rays; to use the resulting cladogram (4) to 
assess the reliability of fossils for recon- 



structing polygyrid phylogeny; (5) to find and 
report the closest polygyrid convergences in 
sympatry on the flat, tridentate, and umbili- 
cate shell forms; (6) to test for retardation of 
evaporative water loss by shell apertural bar- 
riers in living Triodopsis tridentata; and (7) to 
assess remaining conservation priorities for 
the Polygyridae from a phylogenetic per- 
spective. 



MATERIALS AND METHODS 

General Phylogenetic Analysis 

Standard phylogenetic methods of charac- 
ter analysis were used (Hennig, 1966; Wiley, 
1 981 ; Wiley et al., 1 991 ; Brooks & McLennan, 
1991). The outgroups used were the type 
genera of the bradybaenids, helminthoglyp- 
tids, thysanophorids, camaenids, and sag- 
dids, plus Cepolis to represent the xanthony- 
cids (Emberton, 1991c). Data sources were 
from anatomical and behavioral characters 
compiled by Emberton (1994a: appendix A), 
with added anatomical character analyses 
using illustrations of Pilsbry (1940), Archer 



POLYGYRID SHELL EVOLUTION 



73 



(1948), Metcalf & Riskind (1979), Pratt 
(1981a), and Emberton (1988a, 1991a), and 
shell character analyses using the collection 
of the Department of Malacology, Academy 
of Natural Sciences of Philadelphia (ANSP). 
Shell characters were limited as much possi- 
ble to those involving complex apertural 
barriers. No anatomy of Pilsbry's (1 940) "Poly- 
gyra plicata group" had ever been ade- 
quately published (W. G. Binney's [1878: 
plate 1 5, fig. I] sketch of the genitalia of "Poly- 
gyra troostiana Lea" is uninformative and un- 
trustworthy, appearing as it does beside a 
totally inaccurate depiction of the genitalia of 
"P. tridentata [Say]"). Therefore, all the (lim- 
ited) ANSP alcohol material of "P. plicata 
Say" was examined, and one adult was cho- 
sen for dissection and illustration of the shell 
and the reproductive system, which were in- 
cluded in the general character analysis. 

Based on experience with anatomical-shell 
comparisons in the context of an anatomical- 
allozymic phylogenetic hypothesis among all 
species of both the Triodopsini and the Me- 
sodontini (Emberton, 1988a, 1991a), anatom- 
ically unknown polygyrid species were tenta- 
tively assigned to subgenus by shell 
characters alone. Thus, subgenus was used 
as the operational taxonomic unit for this 
phylogenetic analysis, even though any given 
subgenus may have been represented by up 
to eleven species that were each scored for 
each character. For this reason, all "autapo- 
morphies" defining subgenera were retained 
in the data matrix. 

Polygyrid allozyme data (Emberton, 1988a, 
1991a, 1994a) were not used in this analysis 
because data were lacking for many subgen- 
era and because existing data were from two 
separate analyses involving only partially 
overlapping sets of loci. Instead, relevant 
portions of this phylogentic hypothesis were 
visually compared for topological congru- 
ency with previously published, allozyme- 
based hypotheses (Emberton, 1988a, 1991a, 
1994a). 

Phylogenetic analysis was conducted by 
hand and was interactive with construction of 
the data matrix. The analysis progressed 
along successively more restricted ingroups, 
each of which was compared with its closest 
possible outgroup. Thus, the resulting cla- 
dogram and its coordinate subgenus-by- 
character-state matrix were superficially free 
of certain homoplasies that would have re- 
sulted from a non-hierarchical, single-out- 
group analysis. 



Taxonomic Revision 

The revision was based on the general 
phylogenetic hypothesis and followed basic 
principles of phylogenetic taxonomy (Queiroz 
& Gauthier, 1990), which are becoming well 
established among vertebrate systematists 
and have recently been introduced to mala- 
cology by Roth (1995). The method, as em- 
ployed here, designates as taxa clades that 
are defined by shared derived characters (sy- 
napomorphies), regardless of subsequent 
evolutionary modifications of those charac- 
ters. For a discussion of the naturalness of 
this method and its great advantages over 
traditional taxonomy, see Queiroz & Gauthier 
(1990). 

Shell-Based Phylogenetic Analysis 

Previous studies had shown the extents 
and limits of intraspecific variation in polygy- 
rid shell morphology (Emberton, 1988a, 
1988b, 1994a, 1994b), which were consid- 
ered during character analysis. In general, 
one intact adult shell of the type species was 
chosen to represent each subgenus, but for 
subgenera with extreme shell variation, two 
or more representative species were se- 
lected. Outgroups were represented by one 
shell each of the type species of the type 
genus of each of the six closest polygyrid 
outgroup families (Emberton, 1991c), except 
when the type genus happened to have a 
highly derived shell morphology. 

Shells were mounted in the planes simul- 
taneously of both the rotational axis and the 
aperture (Emberton, 1988a: fig. 29b, d) on 
clear acetate sheets using thick rubber ce- 
ment, then x-rayed over single-coat SR-5 In- 
dustrex R film. Contact prints were made 
from the x-ray negatives. Shell "apertures" at 
half-whorl intervals were drawn, with accom- 
panying 3-mm scale lines, from the contact 
prints using a camera lucida mounted on a 
Wild M-5 dissecting microscope. The draw- 
ings were inked, reduce-xeroxed until all of 
about the same size, and mounted in regular 
array, arranged by a former classification 
(Webb, 1974; Richardson, 1986) that has 
since been revised (Emberton, 1994a, this 
paper). 

The demounted shells themselves, as well 
as the x-ray drawings of their ontogenies, 
were compared in a standard phylogenetic 
character analysis (Wiley, 1981; Wiley et al., 
1991; Brooks & McLennan, 1991: chapter 2). 



74 



EMBERTON 



Conchological differences known to occur 
among closely related species within sub- 
genera of the Triodopsini and the Mesodon- 
tini (Emberton, 1988a, 1991a) were dis- 
counted as characters. 

The resulting shell-character by subgenus 
matrix was analyzed phylogenetically using 
Hennig86 (Farris, 1988), assigning equal 
weights to all characters. A Nelson semi- 
strict consensus tree (Farris, 1988) was com- 
puted from the set of resulting, equally and 
maximally parsimonious cladograms. 

Reliability of Fossils 

To qualitatively assess the reliability of fos- 
sils for reconstructing polygrid phylogeny, 
the shell-based and anatomy-behavior-shell- 
based phylogenetic hypotheses were com- 
pared for their degrees of phylogenetic res- 
olution among subgenera. Resolution in both 
cases was quantified as the number of nodes 
relative to the maximum number of possible 
nodes for the given number of taxa. 

Closest Convergences in Sympatry 

Closest potential polygyrid shell conver- 
gences in sympatry on the flat, tridentate, and 
umbilicate shell forms were searched for us- 
ing Pilsbry (1940), Hubricht (1985), and the 
collections of the Field Museum of Natural 
History, Chicago. Actual sympatry was tested 
by field work conducted during the spring 
months of 1979, 1981, 1982, and 1983. 

Shell Barriers and Water Loss 

Twenty-five adult Triodopsis tridentata 
were collected during five field trips in the 
spring and fall of 1970. Twenty-three were 
from Athens County, Ohio, and two from 
Monongahela County, West Virginia. Initial 
weights ranged from 0.39 to 1 .06 gm. From 
ten of these snails, all three apertural denti- 
cles were completely removed using a table- 
mounted dentist's drill. These barrier-less 
nails were given 20 hours to recuperate from 
the operation, and seven appeared at that 
time to be uninjured and normally active. 

All snails were weighed and placed into in- 
dividual rubber-stoppered Erienmeyer flasks 
in which were suspended 1 0.0 gm of the des- 
iccant calcium sulfate in a cheesecloth bag. 
Temperature was maintained at 14-15"C in a 
walk-in refrigerator. Each snail was weighed 
on a tortion balance every hour for 18 hours. 



Weighing took about two minutes per snail. 
At each weighing, the snail's activity state 
was recorded as (a) fully extended, (b) par- 
tially extended, (c) retracted without epi- 
phragm, (d) retracted with partial epiphragm, 
or (e) retracted with complete epiphragm. Pe- 
riods of individual fully extended activity were 
also recorded when they occurred between 
weighings. 

Each recorded weight was expressed as a 
percentage of the snail's initial weight, then 
the percent decrease from the previous 
hour's weight was calculated for each "snail- 
hour" that proved usable. Mean percent de- 
creases were calculated for each of eight ap- 
erture/activity categories. Differences among 
categories were expressed as percent 
changes in rates of evaporative water loss. 
The study was conducted some 25 years 
ago, and since that time the raw data were 
lost, so no statistical analysis could be per- 
formed. 

Remaining Conservation Priorities 

Phylogeny-based conservation priorities 
were assessed for the categories of (1) radi- 
ating, endemic clades; (2) extremely autapo- 
morphic, endemic taxa; (3) relic sister groups 
to major clades; and (4) sites rich in conver- 
gences in sympatry (Emberton, 1992). Prior- 
ities in these categories were judged from the 
general polygyrid phylogenetic hypothesis/ 
revision (this paper; Emberton, 1988a, 1991a) 
and from known species distributions (Hu- 
bricht, 1985) and sites of known high diver- 
sity (Solem, 1976; Emberton, 1995c, unpub- 
lished; Hubricht, unpublished). The current 
conservation status of each high-priority 
taxon or site was evaluated based on the 
U.S. Federal Endangered Species List and 
the locations of national and regional parks 
and forest preserves. 



RESULTS 

General Phylogenetic Analysis 

Table 1 defines the 1 1 5 characters used for 
phylogenetic analysis, with references to il- 
lustrations of the characters. I had not previ- 
ously used or detected some of these char- 
acters (39, or 34%) (Emberton, 1 988a, 1 991 a, 
1994a), primarily those dealing with (a) penial 
morphology within the tribe Stenotremini 
(Fig. 3), (b) reproductive-system morphology 



POLYGYRID SHELL EVOLUTION 75 

TABLE 1. Anatomical, behavioral, and shell characters used for a phylogenetic hypothesis (Fig. 8) and 
a revision (text) of the Polygyridae. Citations refer to papers of Emberton, unless otherwise indicated. 

1. Nodulose fertilization pouch-seminal receptacle complex (1994a: fig. 2: character-state 2.2). 

2. Anteriorly united retractor muscles (1994a: fig. 2: character-state 3.2). 

3. Deeply excavated ureteric interramus (1994a: fig. 2: character-state 4.2). 

4. Single, dorsal, penial pilaster (1994a: fig. 2: character-state 5.2). 

5. Proximally swollen, internally lamellate vas deferens (1994a: fig. 2: character-state 8.2). 

6. Terminally papillate penial verge (1988a: figs. 2f, 3b, 4b, 5e, 7b, 7d, 8c). 

7. Two, flat terminal papillae on a terminal penial verge (1988a: fig. 6a). 

8. Distinct but pustulate lappets (= transversely, partially fused pustules) on the penial pilaster 
(1988a: figs. 2b, 5c, 5f). 

9. Doubled density of pustulate lappets on the penial pilaster (1988a: figs. 5a, 5d). 

10. Smooth lappets (= transversely, completely fused pustules) on the penial pilaster (1988a: fig. 
2e). 

11. Halved density of smooth lappets on the penial pilaster (1988a: figs. 2d, 4a). 

12. Smooth penial-pilastral lappets, plus in adulthood a short vas deferens (only about twice as 
long as the penis) and a penial-retractor-muscle attachment near the penis (on the vas deferens 
within one-third penis-length of the apex of the penis) (1988a: table 4). 

13. Greatly enlarged pustules on the penial pilaster (1988a: fig. 7). 

14. Penial-wall columns that merge mid-ventrally into 6-10 U-shapes that are tapered and slightly 
separated and that bear unequally sized pustules (1988a: fig. 8). 

15. Penial-pilastral pustules forming a single column of abutting cubes (1988a: fig. 8a). 

16. A ventrally subterminal penial verge (1988a: fig. 7). 

17. Penial-pilastral pustules that are knob-like, unfused, and abruptly larger than the penial-wall 
pustules (1988a: figs. 9a, 9c), or derivatives thereof. 

18. 15-20 penial-wall columns unmerging and radiating directly from the ejaculatory pore (1988a: 
figs. 9a, 9c), or derivatives thereof. 

19. Club-shaped penis with a ventrally subterminal ejaculatory pore about 1/5-way from the apex 
and indented into the penial wall (Webb, 1959: figs. 22, 27, 34, 38; 1988a: fig. 9), or derivatives 
thereof (characters 28-30). 

20. Penial-pilastral pustules fused into two interdigitating columns of rectangular boxes (1 988a: fig. 
12). 

21. Penial-pilastral polygons 4-10 times the size of penial-wall pustules and armed with pustule- 
sized knobs, or derivatives thereof (characters 22-24). 

22. Penial-pilastral polygons fused into a single mass or into large, irregular masses (1 988a: fig. 1 1 ). 

23. Ventral penial-wall columns with pustules indistinct (1988a: fig. 11). 

24. Penial pilaster 3/4 the length of the penis and bearing polygons armed with blunt spurs (1988a: 
figs. 13a, 14a, 14b, 16a). 

25. Indistinct pustules on the ventral-most radiating penial-wall columns (1988a: fig. 18b). 

26. Penial-wall columns merging mid-ventrally into 5-7 acute, equilateral, widely separated 
V-shapes bearing equally sized pustules (1988a: figs. 14a, 15b, 16a). 

27. Extremely long, narrow penis (at least 25 times as long as wide) (1988a: fig. 13). 

28. Mace-shaped penis with a ventrally subterminal ejaculatory pore and with a sub-pore region 
erectile as a fleshy peduncle, and derivations thereof (characters 29, 30). 

29. Ejaculatory-pore position approximately 1/4-way from the penial apex, peduncle small (Webb, 
1948: fig. 4; Webb, 1959: figs. 14, 25a, 40, 43; 1988a: figs. 14a-b, 15-17). 

30. Ejaculatory-pore position approximately 2/5-way from the penial apex, peduncle large (Webb, 
1959: figs. 12, 13, 15, 41; 1988a: figs. 14c-d, 18a, 18c). 

31. A discernible clasping disc during mating (1994a: fig. 2: character-state 1.4), or derivatives 
thereof. 

32. An unfanned origin of the penial retentor muscle (1994a: fig. 2: character-state 7.3). 

33. An epiphallus and flagellum (1994a: fig. 2: character-state 9.2), or derived loss thereof. 

34. A constriction in the epiphallus from the penial apex part-way toward the flagellum (1994a: fig. 
2: character-state 9.3). 

35. A fleshy protuberance near the apex of the penis (Roth & Miller, 1992: fig. 6). 

{continued) 



76 EMBERTON 

TABLE 1. Anatomical, behavioral, and shell characters used for a phylogenetic hypothesis (Fig. 8) and 
a revision (text) of the Polygyridae. Citations refer to papers of Emberton, unless otherwise indicated. 
(Continued) 

36. Conical, non-papillate verge at the apex of the penis (Pilsbry, 1940: fig. 512Bb; Webb, 1970: 
plate 35, fig. 5; Roth & Miller, 1993: figs. 19, 24). 

37. Clasping disc during mating that is as voluminous as the inserted portion of the penis (1994a: 
fig. 2: character-state 1.5), or derivatives thereof. 

38. Minutely pustulate sculpture on the dorsal penial wall (1994a: fig. 2: character-state 5.4). 

39. Paired dorsal penial pilasters (Pilsbry, 1940: fig. 496Aa, Bb', D), or derivative thereof (character 
42). 

40. Rugose clasping disk (Webb, 1990: plate 6, figs. 1-4). 

41. Nearly effaced paired dorsal pilasters (1994a: appendix B, character state 5.4). 

42. Single dorsal pilaster, plus a clasping disc that is twice as voluminous as the inserted porlion 
of the penis (1994a: fig. 2: character-state 1.5). 

43. One or more small, pointed, fleshy processes on the clasping disc, and derivatives thereof 
(characters 44, 45). 

44. A single large, pointed, fleshy process on the clasping disc (Pilsbry, 1940: fig. 506, Id-e; Webb, 
1948: figs. 3, 3a). 

45. Two large, pointed, fleshy processes on the clasping disc (Pilsbry, 1940: fig. 510: 2a, 5a). 

46. Clasping disc divided peripherally into two or three broad, unpointed lobes (Webb, 1965: plate 
27, figs. 1-4). 

47. Epiphallus longer than the prostate-uterus (Pilsbry, 1940: figs. 524, 525). 

48. Chitinous, ornate spermatophore (Webb, 1954). 

49. No penial insertion during mating (1994a: fig. 2: character-state 1.8). 

50. Lateral pilaster(s) on the clasping disc (= basal penis) (1994a: fig. 2: character-state 5.5). 

51. A (secondarily) slender spermathecal duct (1994a: fig. 2: character-state 10.4). 

52. (Basal) penial lateral pilasters apically modified into two fleshy-walled cups half as long as the 
penis (Fig. 3E). 

53. Shell aperture with a complete basal lamella having a central trough half or more as broad as 
the lamella, and derivatives thereof. 

54. Shell bearing a straight, even-height parietal apertural denticle isolated from both the umbilicus 
and the aperture (Fig. 6: character-state 5a), and derivatives thereof. 

55. During mating, bearing an everted female organ that receives ejaculate from a pocket at tip of 
the penis (1994a: fig. 2: character-state 1.8). 

56. Apertural-basal-lamellar central trough about one-third or less as broad as the lamella (Fig. 6: 
character-state 4b), and derivatives thereof. 

57. Parietal apertural denticle extending from the umbilicus into the aperture (Fig. 6: character-state 
5b), and derivatives thereof. 

58. A single penial lateral pilaster apically modified into a symmetrical, fleshy-walled cup one-third 
as long as the penis, with a medial branch leading to a medial fleshy protuberance (Fig. 3C). 

59. Lower apertural shell lip joined to the basal body whorl as a thin callus (Fig. 5, character-state 
3b), and derivatives thereof. 

60. Two large, fleshy penial lateral pilasters, both bearing apical V- or U-shaped structures, one up 
and one down (Fig. ЗА). 

61 . Two large, fleshy penial lateral pilasters, neither bearing apical V- or U-shaped structures, and 
one or none bearing an apical, cup-like depression (Fig. 3T, S, P), and derivatives thereof. 

62. One of the two large, fleshy penial lateral pilasters bearing an apical, cup-like depression about 
one-tenth as long as the penis (Fig. 3T). 

63. The two large, fleshy penial lateral pilasters free of apical, cup-like structures (Fig. 3S). 

64. One of the two large, fleshy penial lateral pilasters bearing an apical, cup-like depression 
one-fifth to one-half as long as the penis (Fig. 3P). 

65. Penial-retractor-muscle insertion on or near penial apex (1994a: fig. 2, character-state 7.5-7.8). 

66. Penial sheath (secondarily) completely absent (1994a: fig. 2, character-state 7.8). 

67. Only a vestigial flagellum near the penial apex (1994a: fig. 2, character-state 9.5), and deriva- 
tives thereof. 

68. Shell bearing a triangular parietal denticle (Fig. 6: character-state 6a), and derivatives thereof. 

69. Ovoviviparity (Pilsbry, 1930a). 

(continued) 



POLYGYRID SHELL EVOLUTION 77 

TABLE 1. Anatomical, behavioral, and shell characters used for a phylogenetic hypothesis (Fig. 8) and 
a revision (text) of the Polygyridae. Citations refer to papers of Emberton, unless otherwise indicated. 
{Continued) 

70. Shell apertural expansion rate abruptly increasing then decreasing such that successive whorls 
are nearly equal in volume (Fig. 6: character-state 2b), and derivatives thereof. 

71 . At least one full whorl of growth beyond the expansion-rate increase (Fig. 6: character-state 
2c-hght). 

72. Shell bearing a V- to U-shaped parietal denticle (Fig. 6: character-state 6b). 

73. Shell with a narrow baso-palatal interdenticular notch (Pratt, 1981a: fig. 31). 

74. Complete loss of pustulation in the penial apex (1994a: fig. 2, character-state 5.6). 

75. A small, sac-like, glandular diverticulum of the lower penis (Fig. 5Ln), and derivatives thereof. 

76. Patches of glandular cells on the penial wall above the diverticulum (Fig. 5Ln). 

77. Penial diverticulum large, one-third to equal the volume of the penis (Fig. 5Lb). 

78. Shell apertural expansion rate (secondarily) regular throughout ontogeny. 

79. A secondary lobe on the penial diverticulum (Fig. 5Lb). 

80. A (secondarily) globose shell with the aperture entirely free of denticles (Pilsbry, 1940: figs. 
425-429). 

81. Adnate penial diverticulum (Fig. 5PrF). 

82. Penial diverticulum long and at least twice the volume of the penis (Fig. 5PrP, PrX). 

83. Shell depressed, broadly umbilicate (Zilch, 1959-1960: fig. 2036). 

84. Spiral, threadlike sculpture on the embryonic shell (Pilsbry, 1940: 689). 

85. A bifurcate or trifúrcate penial retractor muscle (Fig. 5PrP). 

86. A vestigial epiphallus without a flagellum (Fig. 5MÍM, MiP). 

87. A slender penis (width < 0.12 length) with an apical, pendant, conical projection (Fig. 5MÍM, 
MiP), and derivatives thereof. 

88. An extremely long and slender penis (width < 0.06 length) (Fig. 5MiM). 

89. A greatly enlarged, muscular, proximal vas deferens (Figs. 7MÍP, 13). 

90. Even-diameter vas deferens with no trace of epiphallus (Fig. 5DD, DU). 

91. A stout penis (length/diameter <3.5) with a straight apex (Fig. 5DU). 

92. A moderately long penis (4 < length/diameter < 10) with a bent or convoluted apex (Fig. 5DD). 

93. A downward curve on the lower limb of the parietal apertural denticle (Pilsbry, 1940: figs. 
384-387). 

94. A raised parietal callus (Pilsbry, 1940: figs. 384-387). 

95. A penial apical chalice formed by the junction of lateral pilasters (1991a: fig. 27). 

96. An even-diameter distal vas deferens with no trace of flagellum or epiphallus (1994a: fig. 2: 
character-state 9.6). 

97. An arched parietal apertural denticle (Fig. 13: character-state 9b), and derivatives thereof. 

98. A depressed, hairless shell (height/diameter 0.4-0.6) (1 991 a: figs. 49, 50), and derivatives thereof. 

99. A regularly oval-shaped aperture with the reflected lip uniform in width throughout its palatal 
and basal regions, with no basal dentition (1991a: fig. 48a). 

100. A basal apertural lamella (1991a: figs. 46, 47). 

101. A pronounced, blade-like parietal apertural denticle (1991a: figs. 46, 47). 

102. A straight basal region of the aperture with only a vestigial lamella (1991a: fig. 10b). 

103. A barrel-shaped, solid pedestal underlying the penial chalice (1991a: fig. 45c-d). 

1 04. A small, globose or subglobose shell (diameter 8-1 5 mm, height/diameter 0.6-0.7) (1 991 a: figs. 
35a, b, 40a, b), and derivatives thereof. 

105. A globose, hairless shell (1991a: figs. 35a, b). 

106. A subglobose shell (height/diameter 0.5-0.6) bearing periostracal scales, with the umbilicus 
broadly covered by an extension of the basal apertural lip, and with palatal and basal apertural 
denticles (1991a: figs. 40a, b), and derivatives thereof. 

107. A thick-walled, hooded, cup-shaped penial chalice (1991a: figs. 7, 8, 9b). 

108. Penial chalice with a higher left than right wall (1991a: fig. 27, transformation 21). 

109. Shell very broadly umbilicate (1991a: figs. 39a,c). 

110. Dorsal penial sculpture (1991a: fig. 28, transformations 31-33). 

111. Dorsal penial sculpture consisting of 4-1 cord-like, subparallel, anastomosing ridges, running 
longitudinally to 30-degrees obliquely (1991a: figs. 4, 6, 16a). 

(continuecf) 



78 



EMBERTON 



TABLE 1. Anatomical, behavioral, and shell characters used for a phylogenetic hypothesis (Fig. 8) and 
a revision (text) of the Polygyridae. Citations refer to papers of Emberton, unless otherwise indicated. 
(Continued) 

1 1 2. Dorsal penial sculpture consisting of 8-1 2 cord-like, subparallel, anastomosing ridges, running 
longitudinally to 30-degrees obliquely, many of which are contiguous with one or both lateral 
pilasters, and many of which enlarge basally to form a network of large basal bulges (1991a: 
figs. 2b, 11b,c, 15c). 

113. Penial chalice a deep, thin-walled scoop, with the left wall much higher than the right (1991a: 
figs. 2b, 11b,c, 15c). 

114. Dorsal penial sculpture consisting of about 8-12 thin parallel ridges, equal in diameter, which 
is constant or gradually increases basally (1991a: figs. 15a,b, 16b,c). 

115. Penial chalice a thick-walled, rounded or pointed ear-like flap, flared to the left (1991a: figs. 
15a,b, 16b,c). 



within the tribe Polygyrini (Figs. 4, 5), and (c) 
shell ontogenetic and apertural morphology 
within — primarily — the tribes Stenotremini 
and Polygyrini (Fig. 6). 

Figure 7 shows the distributions of all 115 
characters among polygyria subgenera (as 
revised below). 

Figure 8 gives the maximum-parsimony 
cladogram of polygyria subgenera (as re- 
vised below), based on the data presented in 
Figure 7. Each node in the cladogram is sup- 
ported by one to three characters, numbered 
as in Table 1. 

Taxonomic Revision 

The following revision exactly follows the 
phylogenetic hypothesis of Figure 8. For 
brevity's sake, definitions employ character 
numbers as defined in Table 1 . Species with 
only tentative assignment to subgenus are 
preceded by a question mark. 

Family POLYGYRIDAE Pilsbry, 1894 

Definition: The first stylommatophoran pul- 
monate gastropod to possess characters #1 , 
2, and 3, and all of its descendants. 



Subfamily TRIODOPSINAE Pilsbry, 1940 

Definition: The first Polygyridae to possess 
characters #4 and 5, and all of its descen- 
dants. 



Tribe TRIODOPSINI 
Definition: as for the subfamily. 



Unnamed Glade Gomprising Webbhelix, 
Neohelix, and Xolotrema 

Synonym: "Xolotrema Rafinesque" (Webb, 
1952) 

Definition: The first Triodopsinae to pos- 
sess character #6, and all of its descendants. 

Genus Webbhelix Emberton, 1988 

Type species: Helix multilineata Say, 1 821 , 
by original designation. 

Definition: The first Triodopsinae to pos- 
sess character #7, and all of its descendents. 

Species: W. multilineata (Say, 1821). 

Genus Neohelix Ihering, 1892 

Type species: Helix albolabris Say, "1816" 
1817, by subsequent designation (Pilsbry, 
1930a). 

Definition: The first Triodopsinae to pos- 
sess character #8, and all of its descendents. 

Subgenus Neohelix (Asamiorbis) subgen. n. 

Type species: Helix dentifera Binney, 1 837. 

Definition: The first Neohelix to possess 
character #9, and all of its descendents. 

Etymology: Dr. Takahiro Asami, land-snail 
ecologist and geneticist, who has worked 
extensively with N. (A.) dentifera and other 
polygyrids in Virginia (Asami, 1988, 1993); or- 
bis (Latin) "disc" or "coil." 

Species: N. (A.) dentifera (Binney, 1837); N. 
(A.) divesta (Gould, 1851); N. (A.) lioderma 
(Pilsbry, 1902). 

Unnamed clade comprising subgenera 

N. (Neohelix) s.s. and 

N. (Solemorbis) subgen. n. 

Definition: The first Neohelix to possess 
character #10, and all of its descendents. 



POLYGYRID SHELL EVOLUTION 



79 




FIG. 3. Character-state analysis of penial-functional-surface anatomy of the Stenotremini; see Table 1, 
characters #52, 58, 60-64. Characters are delineated by solid lines; arrows are hypothesized transforma- 
tions among characters. Anatomical figures (at different size scales) are from Archer (1948). A, Stenotrema 
(Archerelix) subgen. п.; С Stenotrema (Cohutta); E, Euchemotrema; P, Stenotrema (Pilsbrelix) subg. п.; S, 
Stenotrema (Stenotrema); T, Stenotrema (Toxotrema); aa, S. altispira altispira; ad, S. altispira depilatum; bb, 
S. barbatum; bd, S. blandianum; bg, S. barbigerum; bv, S, brevipila; cd, S. caddoense; ch, S. cohuttense; 
dc, S. deceptum; eg, S. edgarianum; ev, S. edvardsi; ex, S. exodon; ext, S. exodon turbinella (= S. turbinella); 
fl, S. florida; ft, E. fraternum; h S. hirsutum; I, S. labrosum, ma, E. monodon aliciae; mg, S. magnifumosum; 
mn, E. monodon, mx, S. maxillatum; pb, S. pilsbryi; pi, S. pilula; sp, S. spinosum; st, S. stenotrema; u, S. 
unciferum. 



80 



EMBERTON 



fpsc 




5mm 




FIG. 4. Reproductive system (minus ovotestis) and shell (umbilical view) of Millerelix (Prattelix) plicata (ANSP 
A2423-A) from Knox County, Tennessee, a = atrium, ag = albumen gland, ap = apical, pendant, conical 
projection of the penis, fpsc = fertilization pouch-seminal receptacle complex (= talon = carrefour), gp = 
gonopore, hd = hermaphroditic duct, mf = mantle-cavity floor, о = oviduvt, p = penis, pr = penial retractor 
muscle, pt = prostate, sd = spermathecal duct (= bursa copulatrix duct = gametolytic duct), u = uterus, v 
= vagina, vd = vas deferens. 



Subgenus Neohelix (Neohelix) s.s. 

Synonym: Neohelix albolabris group (Em- 
berton, 1988). 

Definition: The first Neohelix to possess 
character #11, and all of its descendents. 

Species: N. (N.) albolabhs (Say, 1817); N. 
(N.) major (Binney, 1837). 



Subgenus Neohelix (Solemorbis) subgen. n. 

Type species: Neohelix solemi Emberton, 
1988. 

Synonym: Neohelix alleni group (Ember- 
ton, 1988). 

Definition: The first Neohelix to possess 
character #12, and all of its descendents. 

Etymology: The late Dr. Alan Solem, long 



POLYGYRID SHELL EVOLUTION 

MiP 



81 




FIG. 5. Character-state analysis of the lower-reproductive-tract anatomy of the Polygyhni; see Table 1, 
characters #75-92. Characters are delineated by solid lines; arrows are hypothesized transformations 
among characters. Anatomical figures (at different size scales) are from Pilsbry (1940), Metcalf & Riskind 
(1979), Pratt (1981a), and this paper (Fig. 4). DD, Daedalochila s.S.; DU, Daedalochila (Upsilodon); G, 
Giffordius; Lb, Lobosculum; Ln, Linisa; MiM, Millerelix s.S.; MiP, Millerelix (Prattelix); Po, Polygyra; PrF, 
Praticolella (Farragutia); PrP, Practicolella (Praticolella); PrX, Praticolella (Filapex); be, Pr. berlandiehana; bu, 
D. burlesoni; ch, D. chisosensis; cr, Po. cereolus; df, Mi. doerfeuilliana; hp, D. hippocrepis; Ip, D. leporina; 
Iw, Pr. lawae; mb, Pr. mobiliana; mp, D. multiplicata; mr, Mi. mooreana; pi, G. pinchoti; pi, Mi. plicata; pu, 
Lb. pústula; sp, Po. septemvolva volvoxis; tm, Ln. tamaulipasensis; tx, Ln. texasiana; uv, D. uvulifera. 



82 



EMBERTON 




FIG. 6. Character analysis of shell morphologies of the Stenotremini and the Polyqyrini; Table 1 characters 
#53, 54, 56, 57, 59, 70-72. 



POLYGYRID SHELL EVOLUTION 83 



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84 



EMBERTON 



-OB 

-ox 
-он 
-от 

-ОС 
-OS 



Bradybaena 

Ce pol is 

Helminthoglypta 

Thysanophora 

Pleurodonte 

Sagda 



outgroups 



4,5- 



1-3- 



I 
13,14- 



19- 



17,18-|-20- 



21-22,23 
24-25 



W Webbhelix 

10-11 — NN Neohelix s.S. 
-\ 12 — NS Neohelix (Solemorbis) 

9 NA Neohelix (Asamiorbis) 

15 — XW Xolotrema (Wilcoxorbis) 

16 — XX Xolotrema s.s. 

TdS Triodopsis (Shelfordorbis) 

TdB Triodopsis (Brooksorbis) 

TdP Triodopsis (Pilsbryorbis) 

TdM Triodopsis (Macmillanorbis) 

26—27 TdH Triodopsis (Haroldorbis) 

28—29 — TdT Triodopsis s.S. 

30 — TdV Triodopsis (VaavolQyorbis) 



Trio- 
dop- 
sini 



34- 



31-33- 



-35 — H 
36 — ^V 
40 



Hochbergellus 
Vespericola 



Vesperi- 
colini 



38- 



-39- 



47,48- 



CB Cryptomastix (Bupiogona) 
CC Cryptomastix s.s. 

I 41 — CM Cryptomastix (Micranepsia) 

I p4 6 Tb Tri 1 obops i s 

42—43—44 — AlA Allogona s.s. 

45 — AID AlloQona (Dysmedoma) 



Allo- 
go- 



-As Ashmunella 



Ashmunellini 



37— 



55- 



52-54- 



49-51- 



E Euchemotrema 

1 г58 SC Stenotrema (Cohutta) 

56,57-| 60 SA Stenotrema (Archerelix) 

59— I 64 — SP Stenotrema (Pilsbrelix) 

61— 1-63— SS Stenotrema s.s. 

62 — ST Stenotrema (Toxotrema ) 



Steno- 
tremini 



69- 



68—1 



71- 



65-67 



76- 



70— I 75— I г79 

77,78-| 81- 



72-74 



86- 



-PO 
-Ln 
-Lb 
-PrF 
80— I 83-PrE 
82-84-PrX 
85-PrP 
87-88-MiM 
1 89-MiP 



95-97- 



90-91-DU 
92-94 DD 

98— г99 PaV 

I 100-lOlPaP 
I 102,103PaR 
-104-rl05 — IH 

I 106 II 

107 F 

I 109 App 

108-1 lllMeA 

110-1-2 ЗМеК 

1145МеМ 



Giffordius 

Pol у дуг a 

Linisa 

Lobos culum 

Praticolella 

Praticolella 

Praticolella 

Praticolella 

Millerelix s.s. 

Millerelix (Prattelix) 

Daedalochila (Upsilodon) 

Daedalochila s.s. 



(Farragutia) 
(Eduardus) 
(Filapex) 
s.S. 



Poly- 
gyrini 



Patera (Ves per patera) 

Patera s.s. 

Patera (Ragsdaleorbis) 

Inflectarius (Hubrichtius) 

Inflectarius s.s. Meso- 

Fumonelix dontini 

Appalachina 

Mesodon (Aphalogona) 

Mesodon (Akromesodon) 

Mesodon s.S. 



FIG. 8. Phylogenetic hypothesis for polygyrid subgenera based on the data in Fig. 7. Synapomorphies 
supporting each node and defining each subgenus are numbered as in Table 1. "23MeK" - 112, 113 MeK. 
"1145MeM" = 114,115 MeM. 



POLYGYRID SHELL EVOLUTION 



85 



one of the world's leading and most prolific 
specialists on land snails, who did some im- 
portant work on polygyrids (Solem, 1976); or- 
bis (Latin) "disc" or "coil." 

Species: N. (S.) alleni (Sampson, 1883); N. 
(S.) solemi Emberton, 1988. 



Genus Xo/ofrema Rafinesque, 1819 

Type species: Helix denotata Férussac, 
1 821 (= Helix notata Deshayes, 1 830) by sub- 
sequent designation (Pilsbry, 1940). 

Definition: The first Triodopsini to possess 
characters #13 and 14, and all of its descen- 
dents. 



Subgenus Xolotrema (Wilcoxorbls) 
Webb, 1952 

Type species: Polygyra appressa fosteri F. 
С Baker, 1932, by original designation. 

Definition: The first Xolotrema to possess 
character #15, and all of its descendents. 

Species: X. (W.) fosteri (F. С Baker, 1932); 
X. (W.) occidentalis (Pilsbry & Ferriss, 1907). 



Subgenus Xolotrema (Xolotrema) s.s. 

Definition: The first Xolotrema to possess 
character #16, and all of its descendents. 

Species: X. (X.) caroliniensis (Lea, 1834); X. 
(X.) denotata (Férussac, 1821); X. (X.) ob- 
stricta (Say, 1821). 



Genus Triodopsis Rafinesque, 1819 

Type species: Helix tridentata Say, "1816" 
1817, by original designation. 

Definition: The first Thodopsinae to pos- 
sess characters #17 and 18, and all of its 
descendants. 



Subgenus Triodopsis (Shelfordorbis) 
Webb, 1959 

Type species: Triodopsis fraudulenta vul- 
gata Pilsbry, 1940, by original designation. 

Synonym: species group Triodopsis vul- 
gata (Emberton, 1988). 

Definition: The first Triodopsis to possess 
character #19, and all of its descendents. 

Species: T (S.) claibornensis Lutz, 1950; T. 
(S.) fraudulenta (Pilsbry, 1894); Г. (S.) picea 
Hubricht, 1958; Г. (S.) vulgata Pilsbry, 1940. 



Subgenus Triodopsis 
(Brooksorbis) subgen. n. 

Type species: Polygyra platysayoides 
Brooks, 1933. 

Synonym: species group Triodopsis 
platysayoides (Emberton, 1988). 

Definition: The first Triodopsis to possess 
character #20, and all of its descendents. 

Etymology: The late Dr. Stanley T. Brooks, 
who described the type species; orbis (Latin) 
"disc" or "coil." 

Species: T. (B.) platysayoides (Brooks, 
1933). 

Unnamed Clade Comprising Triodopsis 

Subgenera T (Pilsbryorbis) subgen. п., T. 

(Macmillanorbis) subgen. п., T. 

(Haroldorbis), T. (Triodopsis), and 7". 

(Vagvolgyorbis) subgen. n. 

Definition: The first Triodopsis to possess 
character #21, and all of its descendents. 

Subgenus Triodopsis (Pilsbryorbis) 

subgen. n. 

Type species: Polygyra tridentata tennes- 
seensis Walker & Pilsbry, 1902. 

Synonym: species groups Triodopsis ten- 
nesseensis and T. burchi (Emberton, 1988a). 

Definition: The first Triodopsis to possess 
characters #22 and 23, and all of its descen- 
dents. 

Etymology: The late Dr. Henry A. Pilsbry, 
for some 70 years the world's best known 
and most productive land-snail specialist, 
who wrote the definitive monograph on poly- 
gyrids (Pilsbry, 1940); orbis (Latin) "disc" or 
"coil." 

Species: T (P.) burchi Hubricht, 1950; T 
(P.) complanata (Pilsbry, 1 898); T (P.) tennes- 
seensis (Walker & Pilsbry, 1902). 

Unnamed Clade Comprising Triodopsis 

Subgenera T (Macmillanorbis) subgen. п., 

Г. (Haroldorbis), T. (Triodopsis), and T. 

(Vagvolgyorbis) subgen. n. 

Definition: The first Triodopsis to possess 
character #24, and all of its descendents. 

Subgenus Triodopsis (IVIacmillanorbis) 

subgen. n. 

Type species: Triodopsis tridentata rugosa 
Brooks & MacMillan, 1940. 

Synonym: species group Triodopsis rug- 
osa (Emberton, 1988). 



86 



EMBERTON 



Definition: The first Triodopsis already hav- 
ing character #24, to possess character #25, 
and all of its descendente. 

Etymology: The late Gordan K. MacMillan 
of the Carnegie Museum, Pittsburg, who col- 
lected and coauthored the type species; or- 
bis (Latin) "disc" or "coil." 

Species: T. (M.) fulciden Hubricht, 1952; T. 
(M.) rugosa Brooks & MacMillan, 1940. 

Unnamed Clade Comprising Triodopsis 

Subgenera T. (IHaroldorbis), T. (Triodopsis), 

and T (Vagvolgyorbis) subgen. n. 

Definition: The first Triodopsis already hav- 
ing character #24, to possess character #26, 
and all of its descendents. 

Subgenus Triodopsis (l4aroldorbis) 
Webb, 1959 

Type species: Triodopsis cragini Call, 
1886, by original designation. 

Synonyms: "Triodopsis copei (Wetherby)" 
(Vagvolgyi, 1968; species group Triodopsis 
cragini Call (Emberton, 1988a). 

Definition: The first Triodopsis already hav- 
ing characters #24 and 26, to possess char- 
acter #27, and all of its descendents. 

Species: T. (H.) cragini Call, 1886; T. (H.) 
Iienriettae (Mazyck, 1877); T (14.) vultuosa 
(Gould, 1848). 

Unnamed Clade Comprising Triodopsis 

Subgenera T (Triodopsis) and T 

(Vagvolgyorbis) subgen. n. 

Definition: The first Triodopsis already hav- 
ing characters #24 and 26, to possess char- 
acter #28, and all of its descendents. 

Subgenus Triodopsis (Triodopsis) s.s. 

Synonym: species groups Triodopsis trl- 
dentata (Say) and T fallax (Say) (Emberton, 
1988a). 

Definition: The first Triodopsis already hav- 
ing characters #24, 26, and 28, to possess 
character #29, and all of its descendents. 

Species group T (T.) tridentata s.S.: T (T.) 
anterldon (Pilsbry, 1940); T (T.) tridentata 
(Say, 1817). 

Species group T. (T.) fallax: T. (J.) alabam- 
ensis (Pilsbn/, 1902); T (T.) fallax (Say, 1825); 
T (T.) hopetonensis (Shuttleworth, 1852); T 
(T.) obsoleta (Pilsbry, 1894); T (T.) palustris 



Hubricht, 1958; T. (T.) soelneri (Henderson, 
1907); T. (T.) vannostrandi (Bland, 1875). 

Subgenus Triodopsis (Vagvolgyorbis) 

subgen. n. 

Type species: Polygyra tridentata juxtidens 
Pilsbry, 1894b. 

Synonym: species group Triodopsis juxti- 
dens (Pilsbry) (Emberton, 1988). 

Definition: The first Triodopsis already hav- 
ing characters #24, 26, and 28, to possess 
character #30, and all of its descendents. 

Etymology: Dr. Joseph Vagvolgyi, author 
of a conchological monograph on the Triod- 
opsinae and Cryptomastix (Vagvolgyi, 1968); 
orbis (Latin) "disc" or "coil." 

Species: T (V.) discoidea (Pilsbry, 1904); T 
(V.) juxtidens (Pilsbry, 1894b); T (V.) neglecta 
(Pilsbry, 1899); T (V.) pendula Hubricht, 
1952. 

Subfamily POLYGYRINAE s.s. 

Definition: The first Polygyridae to possess 
characters #31 , 32, and 33, and all of its de- 
scendents. 

Tribe VESPERICOLINI Emberton, 1994 

Type genus: Vespericola Pilsbry, 1939, by 
original designation. 

Definition: The first Polygyrinae to possess 
character #34, and all of its descendents. 

Genus Hochbergellus Roth & Miller, 1992 

Type species: Hochbergellus hirsutus Roth 
& Miller, 1992, by original designation. 

Definition: The first Vespericolini to pos- 
sess character #35, and all of its descen- 
dents. 

Species: H. hirsutus Roth & Miller, 1992. 

Genus Vespericola Pilsbry, 1939 

Type species: Polygyra columbiana pilosa 
Henderson, 1928, by original designation. 

Definition: The first Vespericolini to pos- 
sess character #36, and all of its descen- 
dents. 

Species: V. armígera (Binney, 1885); V. co- 
lumbianus (Lea, 1838); V. euthales (Berry, 
1939); V. hapla (Berry, 1933); V. karokorum 
Talmadge, 1962; V. marinensis Roth & Miller, 
1993; V. megasoma (Dall, 1905); "I/, sp. n. 1" 
(Roth & Miller, 1993); "I/, sp. n. 2" (Roth & 
Miller, 1993); V. orius (Berry, 1933); V. pilosus 



POLYGYRID SHELL EVOLUTION 



87 



(Henderson, 1928); У. pinícola (Berry, 1916); 
V. pressleyl Roth, 1985; V. shasta (Berry, 
1921); V. slerrana (Berry, 1921). 

Unnamed Glade Comprising Tribes 

Allogonini and Ashmunellini and 

Infrafamily Polygyrinai 

Definition: The first Polygyrinae to possess 
character #37, and all of its descendents. 

Tribe ALLOGONINI Emberton, 1994 

Type genus: Allogona Pilsbry, 1939, by 
original designation. 

Definition: The first Polygyrinae already 
having character #37, to possess character 
#38, and all of its descendents. 

Genus Cryptomastix Pilsbry, 1939 

Type species: Polygyra mullani oineyae 
Pilsbry, 1928, by original designation. 

Synonym: Triodopsis Rafinesque (in part) 
(Pilsbry, 1940; Vagvolgyi, 1968). 

Definition: The first Allogonini to possess 
character #39, and all of its descendents. 

Subgenus C. (Buplogona) Webb, 1970 

Type species: Polygyra mullani hendersoni 
Pilsbry, 1928, by original designation. 

Definition: The first Cryptomastix to pos- 
sess character #40, and all of its descen- 
dents. 

Species: С (В.) hendersoni (Pilsbry, 1928). 

Subgenus C. (Cryptomastix) s.s. 

Definition: (as for the genus). 

Species: С (С.) dévia (Gould, 1846); С. (С.) 
mullani (Bland & Cooper, 1862); С. (С.) san- 
burni (Binney, 1886). 



Genus Л//одопа Pilsbry, 1939 

Type species: Helix profunda Say, 1821 , by 
original designation. 

Definition: The first Allogonini already hav- 
ing character #42, to possess character #43, 
and all of its descendents. 



Subgenus A. (Allogona) s.s. 

Definition: The first Allogonini to possess 
character #44, and all of its descendents. 
Species: A (A.) profunda (Say, 1821) 

Subgenus A. (Dysmedoma) Pilsbry, 1 939 

Type species: Helix townsendlana Lea, 
1838, by original designation. 

Definition: The first Allogonini to possess 
character #45, and all of its descendents. 

Species: A. (D.) lombarda Smith, 1943; A. 
(D.) ptycfiopfiora (Brown, 1870); A. (D.) 
townsendlana (Lea, 1838). 

Genus Trilobopsis Pilsbry, 1939 

Type species: Helix lorlcata Gould, 1846, 
by original designation. 

Definition: The first Allogonini already hav- 
ing character #42, to possess character #46, 
and all of its descendents. 

Species: T. lorlcata (Gould, 1846); T. penl- 
tens (Hanna & Rixford, 1923); T. roperi (Pils- 
bry, 1889); T. tehiamana (Pilsbry, 1928); T. tra- 
chypepla (Berry, 1933). 

Tribe ASHMUNELLINI Webb, 1954 

Type genus: Ashmunella Pilsbry & Cocker- 
ell, 1899, by original designation. 

Definition: The first Polygyrinae already 
having character #37, to possess characters 
#47 and 48, and all of its descendents. 



Subgenus С (Micranepsia) Pilsbry, 1940 

Type species: Helix germana Gould, 1851, 
by original designation. 

Definition: The first Cryptomastix to pos- 
sess character #41, and all of its descen- 
dents. 

Species: С (M.) germana (Gould, 1851). 

Unnamed Clade Comprising Allogona 
and Trilobopsis 

Definition: The first Allogonini to possess 
character #42, and all of its descendents. 



Genus Ashimunella Pilsbry & Cockerell, 
1899 

Type species: Polygyra miortiyssa Dall, 
1898 [= Ashmunella rhyssa miorhyssa (Dall, 
1898)], by subsequent designation (Pilsbry, 
1905). 

Definition: (as for the tribe). 

Species (n = 49): A. altissima (Cockerell, 
1898); A. angulata Pilsbry, 1905; A. ani- 
masensis Vagvolgyi, 1974; A. ashmuni (Dall, 
1896); A. auriculata (Say, 1818); A. bequaerti 
Clench & Miller, 1966; A. binneyl Pilsbry & 
Ferriss, 1917; A. carlbadensis Pilsbry, 1932; 



88 



EMBERTON 



A. chiricahuana (Dall, 1 896); A. cockerelli Pils- 
bry & Ferriss, 1917; A. danieisi Pilsbry & Fer- 
riss, 1915; A. edithae Pilsbry & Cheatum, 
1 951 ; A. esuhtor Pilsbry, 1 905; A. ferrissi Pils- 
bry, 1905; A. harhsi Metcalf & Smartt, 1977; 
A. hawleyi Metcalf, 1 973; A. hebardi Pilsbry & 
Vanatta, 1923; A. inthcata Pilsbry, 1948; A. 
jamesensis Metcalf, 1973 (fossil); A. juarezen- 
sis Pilsbry, 1948; A. kochi Clapp, 1908; A. 
lenticula Gregg, 1953; Л. lepidoderma Pilsbry 
& Ferriss, 1910; A levettei (Bland, 1881); A 
macromphala Vagvolgyi, 1974; A. mearnsi 
(Dall, 1896); A. mendax Pilsbry & Ferriss, 
1917; A. meridionalis Pilsbry, 1948; A. mog- 
ollonensis Pilsbry, 1900; A. montivaga Pils- 
bry, 1948; A. mudgei Cheatum, 1971; A. or- 
ganensis Pilsbry, 1936; A. pasonis (Drake, 
1951); A. pilsbryana Ferriss, 1914; A. próxima 
Pilsbry, 1 905; A. pseudodonta (Dall, 1 897); A. 
rhyssa (Dall, 1897); A. rileyensis Metcalf & 
Hurley, 1971; A. ruidosana Metcalf, 1973 
(fossil); A. salinasensis Vagvolgyi, 1974; A. 
sprouli Fullington & Fullington, 1978; A. tegil- 
lum Metcalf, 1973; A. tetrodon Pilsbry & Fer- 
riss, 1915; A. thomsonlana (Ancey, 1887); A. 
todseni Metcalf & Smartt, 1977; A. tularosana 
Metcalf, 1973; A. varicifera Ancey, 1901; A. 
walken Ferriss, 1904; A. watleyi Metcalf & 
Fullington, 1978. 

Infrafamily POLYGYRINAI s.s. 

Definition; The first Polygyrinae already 
having character #37, to possess characters 
#49, 50, and 51, and all of its descendents. 

Tribe STENOTREMINI Emberton, 1994 

Type genus: Stenotrema Rafinesque, 
1819. 

Definition: The first Polygyrinai to possess 
characters #52, 53, and 54, and all of its de- 
scendents. 

Genus Euchemotrema Archer, 1939 

Type species: Helix monodon Rackett, 
1821, by subsequent designation (Pilsbry, 
1940). 

Definition: The first Stenotremini to pos- 
sess character #55, and all of its descen- 
dents. 

Species: E. fasciatum (Pilsbry, 1940); E. 
fraternum (Say, 1824); E. hubrichti (Baker, 
1937); E. leai (Binney, 1840); E. monodon 
(Rackett, 1821); E occidaneum Roth & Em- 



berton, 1994 (early Miocene fossil); E wichi- 
torum Branson, 1972. 



Genus Stenotrema Rafinesque, 1819 

Type species: Stenotrema convexa 
Rafinesque, 1819 [nomen nudum = Helix 
stenotrema Pfeiffer, 1842]. 

Definition: The first Stenotremini to pos- 
sess characters #56 and 57, and all of its 
descendents. 



Subgenus Stenotrema (Cohutta) 
Archer, 1948 

Type species: Polygyra cohuttensis Clapp, 
1914, by original designation. 

Definition: The first Stenotrema to possess 
character #58, and all of its descendents. 

Species: S. (Cohutta) cohuttensis Archer, 
1948 



Unnamed Clade Comprising Stenotrema 

(Archerelix), S. (Pilsbrelix), S. (Stenotrema) 

s.S., and S. (Toxotrema) 

Definition: The first Stenotrema to possess 
character #59, and all of its descendents. 



Subgenus Stenotrema (Archerelix) 

subgen. n. 

Type species: Helix barbigera Redfield, 
1856. 

Description: The first Stenotrema to pos- 
sess character #60, and all of its descen- 
dents. 

Etymology: The late Dr. Allan F. Archer, 
who contributed "information, notes, and 
manuscript" (Archer, 1948: 8) to Pilsbry's 
(1940) monograph on Stenotrema and wrote 
a revision and ecological manual on the ge- 
nus (Archer, 1948); helix (Latin) "coil" or 
"snail." 

Species: S. (A.) barbigerum (Redfield, 
1856); S. (A.) edgarianum (Lea, 1841); S. (A.) 
edvardsi (Bland, 1858); S. (A.) pilsbryi (Fer- 
riss, 1900). 

Unnamed Clade Comprising S. (Pilsbrelix), 
S. (Stenotrema) s.S., and S. (Toxotrema) 

Definition: The first Stenotrema to possess 
character #61, and all of its descendents. 



POLYGYRID SHELL EVOLUTION 



89 



Subgenus S. (Toxotrema) Rafinesque, 1819 

Type species: Helix hirsuta Say, 1817, by 
subsequent designation (Pilsbry, 1930). 

Definition: The first Stenotrema to possess 
character #62, and all of its descendents. 

Species: S. (T.) barbatum (Clapp, 1904); S. 
(T.) hirsutum (Say, 1817); S. (T.) labrosum 
(Bland, 1862); ?S. (T.) simile Grinnnn, 1971. 



Subgenus Stenotrema (Stenotrema) s.s. 

Synonyms: Stenotrema (Stenostoma) 
Rafinesque, 1831 (Archer, ^ 948); Stenotrema 
(Maxillifer) Pilsbry, 1940 (Archer, 1948); 
Stenotrema (Coracollatus) Archer, 1948. 

Definition: The first Stenotrema to possess 
character #63, and all of its descendents. 

Species and subspecies: S. (S.) altispira 
(Pilsbry, 1894); S. (S.) altispira depllatum 
(Pilsbry, 1895); ?S. (S.) angellum Hubricht, 
1958; S. (S.) brevipila (Clapp, 1907); S. (S.) 
caddoense (Archer, 1935); ?S. (S.) 
calvescens Hubricht, 1961 ; S. (S.) florida Pils- 
bry, 1940; S. (S.) magnifumosum (Pilsbry, 
1900); S. (S.) maxillatum (Gould, 1848); ?S. 
(S.) morosum Hubricht, 1978 (Pleistocene- 
Recent fossil); S. (S.) pilula (Pilsbry, 1900); S. 
(S.) spinosum (Lea, 1831); S. (S.) stenotrema 
(Pfeiffer, 1842); S. (S.) unciferum (Pilsbry, 
1 900); ?S. (S.) waldense Archer, 1 938. 



Subgenus Stenotrema (Pilsbrelix) 

subgen. n. 

Type species: Polygyra stenotrema exodon 
Pilsbry, 1900. 

Description: The first Stenotrema to pos- 
sess character #64, and all of its descen- 
dents. 

Etymology: The late Dr. Henry A. Pilsbry, 
who wrote the definitive monograph on poly- 
gyrids (Pilsbry, 1940), and who described the 
type species; helix (Latin) "coil" or "snail." 

Species: S. (P) blandianum (Pilsbry, 1903); 
S. (P) deceptum (Clapp, 1905); S. (P.) exodon 
(Pilsbry, 1900); S. (P) turbinella (Clench & Ar- 
cher, 1933). 



Tribe POLYGYRINI s.s. 

Definition: The first Polygyhnai already 
having characters #65, 66, and 67, to pos- 
sess character #68, and all of its descen- 
dents. 

Genus Giffordius Pilsbry, 1 930 

Type species: Giffordius pinchioti Pilsbry, 
1930, by original designation. 

Definition: The first Polygyhni to possess 
character #69, and all of its descendents. 

Species: G. corneliae Pilsbry, 1930; G. pin- 
choti Pilsbry, 1930. 

Unnamed Clade Comprising Polygyra, 

Linisa, Lobosculum, Praticolella, Millerelix, 

and Daedalochila 

Definition: The first Polygyhni to possess 
character #70, and all of its descendents. 

Genus Polygyra Say, 1818 

Type species: Polygyra septemvolva Say, 
1818, by subsequent designation (Herr- 
mannsen, 1847). 

Definition: The first Polygyhni already hav- 
ing character #70, to possess character #71 , 
and all of its descendents. 

Species: P. caloosaensis Johnson, 1899 
(Pliocene fossil); P. cereolus (Mühlfeld, 1818); 
P. paludosa (Wiegmann, 1839); P. plana 
(Dunker, 1843); P. septemvolva Say, 1818. 

Unnamed Clade Comprising Linisa, 

Lobosculum, Praticolella, Millerelix, 

and Daedalochila 

Definition: The first Polygyhni already hav- 
ing character #70, to possess characters 
#72, 73, and 74, and all of its descendents. 

Unnamed Clade Comprising Linisa, 
Lobosculum, and Praticolella 

Definition: The first Polygyhni already hav- 
ing characters #70, 72, 73, and 74, to pos- 
sess character #75, and all of its descen- 
dents. 



Unnamed Clade Comphsing Polygyhni 
and Mesodontini 

Definition: The first Polygyrinai to possess 
characters #65, 66, and 67, and all of its de- 
scendents. 



Genus Linisa Pilsbry, 1 930 

Type species: Helix (Polygyra) anilis Gabb, 
1865, by original designation. 

Synonyms (fide Pratt, 1981a): Polygyra 
(Daedalochila) texasiana group (in part) (Pils- 



90 



EMBERTON 



bry, 1940); Polygyra (Erymodon) Pilsbry, 
1956; Polygyra (Monophysis) Pilsbry, 1956; 
Polygyra (Solidens) Pilsbry, 1956; Polygyra 
(Linisia) (Pratt, 1981a,b); Daedalochila (in 
part) (Richardson, 1986). 

Definition; The first Polygyrini already hav- 
ing characters #70, 72, 73, 74, and 75, to 
possess character #76, and all of its descen- 
dente. 

Species; ?L. adamnis (Dall, 1890) (Upper 
Oligocène fossil); L. albicostulata (Pilsbry, 
1896); L anilis (Gabb, 1865); ?L. aula- 
comphala (Pilsbry & Hinkley, 1907); L. behri 
(Gabb, 1865); ?L. bicruris (Pfeiffer, 1857); ?L. 
cantralli (Solem, 1957); ?L. couloni (Shuttle- 
worth, 1852); ?L. dissecta (Martens, 1892); 
?L. dysorii (Shuttleworth, 1852); ?L. euglypta 
(Pilsbry, 1896); ?L hertlemi Haas, 1961; ?L. 
hindsii (Pfeiffer, 1845); ?L. idiogenes (Pilsbry, 
1956); ?L. matermontana (Pilsbry, 1896); ?L. 
nelson! (Dall, 1897); L. pergrandis (Solem, 
1959); ?L. plagioglossa (Pfeiffer, 1859); L. 
polita (Pilsbry & Hinkley, 1907); ?L. ponsonbyi 
(Pilsbry, 1896); L. richardsoni (Martens, 
1892); ?L. suprazonata (Pilsbry, 1900); L. 
tamaulipasensis (Lea, 1867); L. texasiana 
(Moricand, 1833); L. ventrosula (Pfeiffer, 
1845); ?L. yucatanea (Morelet, 1853). 

Unnamed Glade Comprising Lobosculum 
and Praticolella 

Definition: The first Polygyrini already hav- 
ing characters #70, 72, 73, 74, 75, and 76, to 
possess characters #77 and 78, and all of its 
descendents. 

Genus Lobosculum Pilsbry, 1930 

Type species; Helix pústula Férussac, 
1822, by subsequent designation (Pilsbry, 
1930b; 320). 

Definition; The first Polygyrini already hav- 
ing characters #72, 73, 74, 75, 76, 77, and 
78, to possess character #79, and all of its 
descendents. 

Species; L. pústula (Férussac, 1822); L. 
pustuloides (Bland, 1858). 

Genus Praticolella Martens, 1892 

Type species; Praticola ocampi Strebel & 
Pfeffer, 1880 (= Helix ampia Pfeiffer, 1866), 
by original designation. 

Definition; The first Polygyrini already hav- 
ing characters #72, 73, 74, 75, 76, 77, 78, to 



possess character #80, and all of its descen- 
dents. 

Subgenus Praticolella (Farragutia) 
Vanatta, 1915 

Type species; Helix mobiliana Lea, 1841, 
by original designation. 

Definition; The first Praticolella to possess 
character #81, and all of its descendents. 

Species; P. (F.) mobiliana (Lea, 1841). 

Unnamed Glade Comprising Praticolella 

(Eduardus), P. (Filapex), and 

P. (Praticolella) s.s. 

Definition; The first Praticolella to possess 
character #82, and all of its descendents. 

Comment; The membership of P. (Eduar- 
dus) in this clade needs to be tested by dis- 
section, because Pilsbry (1936) was inexplicit 
about the size of the appendix. 

Subgenus Praticolella (Eduardus) 
Pilsbry, 1930 

Type species; Polygyra martensiana Pils- 
bry, 1907, by original designation. 

Definition; The first Praticolella already 
having character #82, to possess character 
#83, and all of its descendents. 

Species; P. (E.) martensiana (Pilsbry, 
1907). 

Subgenus Praticolella (Filapex) Pilsbry, 1940 

Type species: Helix jejuna Say, 1821, by 
original designation. 

Definition: The first Praticolella already 
having character #82, to possess character 
#84, and all of its descendents. 

Species: P. (F.) bakeri (Vanatta, 1915); P. 
(F.) jejuna (Say, 1821); P. (F.) lawae (Lewis, 
1874). 

Subgenus Praticolella (Praticolella) s.s. 

Definition: The first Praticolella already 
having character #82, to possess character 
#85, and all of its descendents. 

Species: P. (P.) ampia (Pfeiffer, 1866); P. 
(P.) berlandieriana (Moricand, 1833); P. (P.) 
candida Hubricht, 1983; P. (P.) flavescens 
(Pfeiffer, 1848); P. (P.) griseola (Pfeiffer, 
1841); P. (P.) pachyloma (Pfeiffer, 1847); P. 
(P.) strebeliana Pilsbry, 1899; P. (P.) taeniata 
Pilsbry, 1940; P. (P.) trimatris Hubricht, 1983. 



POLYGYRID SHELL EVOLUTION 



91 



Unnamed Clade Comprising Millerelix 
and Daedalochila 

Definition: The first Polygyrini already hav- 
ing characters #70, 72, 73, and 74, to pos- 
sess character #86, and all of its descen- 
dents. 

Genus Millerelix Pratt, 1981 (see below) 

Type species: Helix mooreana W. G. Bin- 
ney, 1857, by original designation. 

Definition: The first Polygyrini already hav- 
ing characters #70, 72, 73, 74, and 86, to 
possess character #87, and all of its descen- 
dents. 

Subgenus Millerelix (Millerelix) s.s. 
Pratt, 1981 

Definition: The first Millerelix to possess 
character #88, and all of its descendents 
(Pratt, 1981b). 

Species: M. doerfeulliana (Lea, 1838); M. 
gracilis (Hubricht, 1961); 7M. implicata (Mar- 
tens, 1865); M. lithica (Hubricht, 1961); M. 
mooreana (Binney, 1857); ?M rhoadsi (Pils- 
bry, 1900); M. tholus (Binney, 1857). 

Subgenus Millerelix (Prattelix) subgen. n. 

Type species: Polygyra plicata Say, 1821. 

Synonyms: Polygyra plicata group (Pilsbry, 
1940); Daedalochila plicata group = unnamed 
subgenus (Pratt, 1981a). 

Definition: The first Millerelix to possess 
character #89, and all of its descendents. 

Comments: The shell of the type species is 
sparsely and evenly covered with long, con- 
spicuous periostracal hairs, seemingly round 
in cross-section and slightly curved at the tip, 
that fade out toward the umbilicus (Fig. 13). 
They are easily broken, hence Pilsbry's 
(1940: 626) mildly erroneous, "a few short 
hairs, usually preserved only in the umbilicus 
and behind the lip." The long hairs were 
found in all four of the Academy of Natural 
Sciences's alcohol-preserved lots of D. pli- 
cata: Alabama, Madison County (ANSP A 
2423-B); Tennessee, Marion County (A 2423- 
C); Tennessee, Knox County (A 2423-A, Fig. 
13); and Kentucky, Barren County (A 2387-B, 
most hairs broken). 

Etymology: The subgenus is named in 
honor of Will Pratt. 

Species: deltoidea (Simpson, 1889); fatigi- 
ata (Say, 1 829); yac/ison/ (Bland, 1866); pere- 
grina (Rehder,^932y, plicata {Say,^82^)■, simp- 



soni (Pilsbry & Ferriss, 1907); troostiana (Lea, 
1838). 

Genus Daedalochila Beck, 1837 

Type species: Helix auriculata Say, 1818, 
by subsequent designation (Herrmannsen, 
1847). 

Definition: The first Polygyrini already hav- 
ing characters #70, 72, 73, 74, and 86, to 
possess character #90, and all of its descen- 
dents. 

Subgenus Daedalochila (Upsilodon) 
Pilsbry, 1930c 

Type species: Helix hippocrepis Pfeiffer, 
1848, by original designation. 

Synonym: Daedalochila (Acutidens) Pils- 
bry, 1956. 

Definition: The first Daedalochila to pos- 
sess character #91, and all of its descen- 
dents. 

Comment: The recurved palatal apertural 
denticle of D. acutidentata also occurs in the 
otherwise very different shell of D. poeyi, so 
does not seem to be a reliable character for 
defining a clade. 

Species: ?D. (U.) acutedentata (Binney, 
1858); D. (U.) burlesoni (Metcalf & Riskind, 
1979); D. (U.) chisosensis (Pilsbry, 1936); D. 
(U.) dalli (Metcalf & Riskind, 1979); D. (U.) hip- 
pocrepis (Pfeiffer, 1848); D. (U.) leporina 
(Gould, 1848); D. (U.) multiplicata (Metcalf & 
Riskind, 1979); ?D. (U.) poeyi (Aguayo & 
Jaume, 1947); D. (U.) sp. n. A (Pratt, 1981a); 
D. (U.) sterni (Metcalf & Riskind, 1979). 

Subgenus Daedalochila (Daedalochila) s.s. 

Synonym: Polygyra auriculata group (Pils- 
bry, 1940). 

Definition: The first Daedalochila to pos- 
sess characters #92, 93, and 94, and all of its 
descendents. 

Comments: The downward curve on the 
lower limb of the parietal apertural denticle is 
a newly discovered synapomorphy. Pratt 
(1981a) stated (without giving evidence) that 
?D. ariadne and ?/W/. implicata are members 
of a new genus; this needs to be investi- 
gated. 

Species: ?D. (D.) ariadne (Pfeiffer, 1848); D. 
(D.) auriculata (Say, 1818); D. (D.) auriformis 
(Bland, 1862); D. (D.) avara (Say, 1818); D. (D.) 
delecta (Hubricht, 1976); D. (D.) hausmani 
(Jackson, 1948); ?D. (D.) oppilata (Morelet, 



92 



EMBERTON 



1849); D. (D.) peninsulae (Pilsbry, 1940); D. 
(D.) postelliana (Bland, 1862); D. (D.) sub- 
clause (Pilsbry, 1899); D. (D.) uvulifera (Shut- 
tleworth, 1852). 

Tribe MESODONTINI Emberton, 1991 

Type genus: Mesodon Férussac, 1821. 

Definition: The first Polygyrinai already 
having characters #65, 66, and 67, to pos- 
sess characters #95, 96, and 97, and all of its 
descendents. 



character #100, to possess characters #102 
and 103, and all of its descendents. 

Species: P. (R.) pennsylvanica (Green, 
1827). 

Genus Inflectarius Pilsbry, 1 940 

Type species: Helix inflects Say, 1821, by 
original designation. 

Definition: The first Mesodontini to pos- 
sess character #104, and all of its descen- 
dents. 



Genus Patera Albers, 1850 

Type species: Helix appressa Say, 1821, 
by subsequent designation Pilsbry, 1930c: 
326). 

Definition: The first Mesodontini to pos- 
sess character #98, and all of its descen- 
dents. 

Subgenus Patera (Vesperpatera) 
Emberton, 1991 

Type species: Polygyra binneyana Pilsbry, 
1899, by original designation. 

Definition: The first Patera to possess char- 
acter #99, and all of its descendents. 

Species: P. (V.) binneyana (Pilsbry, 1899); 
P. (V.) clenchi (Rehder, 1932); P. (V.) indian- 
orum (Pilsbry, 1899); P. (V.) kiowaensis (Sim- 
pson, 1888); P. (V.) leathenA/oodi (Pratt, 
1971); P. (V.) roemeri (Pfeiffer, 1848). 

Unnamed Clade Comprising P. (Patera) and 
P. (Ragsdaleorbis) 

Definition: The first Patera to possess char- 
acter #100, and all of its descendents. 

Subgenus Patera (Patera) s.s. 

Definition: The first Patera already having 
character #100, to possess character #101, 
and all of its descendents. 

Species: P. (P.) appressa (Say, 1821); P. 
(P.) clarki (Lea, 1858); P. (P.) laevior (Pilsbry, 
1940); P. (P.) panselena (Hubricht, 1976); P. 
(P.) perigrapta (Pilsbry, 1894b); P. (P.)sargen- 
tiana (Johnson & Pilsbry, 1892). 

Subgenus Patera (Ragsdaleorbis) 
Webb, 1954 

Type species: Helix pennsylvanicus Green, 
1827, by original designation. 
Definition: The first Patera already having 



Subgenus Inflectarius (Hubricfitius) 
Emberton, 1991 

Type species: Mesodon kalmianus Hu- 
bricht, 1965, by original designation. 

Definition: The first Inflectarius to possess 
character #105, and all of its descendents. 

Species: /. (H.) downieanus (Bland, 1861); /. 
(H.) kalmianus (Hubricht, 1965) 

Subgenus Inflectarius (Inflectarius) s.s. 

Definition: The first Inflectarius to possess 
character #106, and all of its descendents. 

Species group /. (I.) edentatus: I. (I.) eden- 
tatus (Sampson, 1889); /. (I.) magazinensis 
(Pilsbry & Ferriss, 1907). 

Species group /. (I.) smithi: I. (I.) smitfii 
(Clapp, 1905). 

Species group /. (I.) inflectus: I. (I.) approx- 
imans (Clapp, 1905); /. (I.) inflectus (Say, 
1821); /. (I.) rugeli (Shuttleworth, 1852); /. (I.) 
verus (Hubricht, 1954). 

Species group: /. (I.) ferrissi: I. (I.) ferrissi 
(Pilsbry, 1897); /. (I.) subpalliatus (Pilsbry, 
1893). 

Genus Fumonelix Emberton, 1991 

Type species: Helix wfieatleyi Bland, 1860, 
by original designation. 

Definition: The first Mesodontini to pos- 
sess character #107, and all of its descen- 
dents. 

Species: F. archeri (Pilsbry, 1940); F. 
ctiristyi (Bland, 1860); F jonesiana (Archer, 
1938); F Orestes (Hubricht, 1975); F. wethi- 
erbyi (Bland, 1874); F. wheatleyi (Bland, 
1860). 

Unnamed Clade Comprising Appalachina 
and Mesodon 

Definition: The first Mesodontini to pos- 
sess character #108, and all of its descen- 
dents. 



POLYGYRID SHELL EVOLUTION 



93 



Genus Appalachina Pilsbry, 1940 

Type species: Polygyra sayana Pilsbry, 
1906, by original designation. 

Definition: The first Mesodontini already 
having character #108, to possess character 
#109, and all of its descendents. 

Species: A. chllhoweensis (Lewis, 1 870); A. 
sayanus (Pilsbry, in Pilsbry & Ferriss, 1906). 

Genus Mesodon Férussac, 1821 

Type species: Helix thyroidus Say, 1817, 
by monotypy. 

Definition: The first Mesodontini already 
having character #108, to possess character 
#110, and all of its descendents. 

Subgenus Mesodon (Aphalogona) 
Webb, 1954 

Type species: Helix elevata Say, 1821, by 
original designation. 

Definition: The first Mesodon to possess 
character #111, and all of its descendents. 

Species: M. (Aph.) elevatus (Say, 1821); M. 
(Aph.) mitchellianus (Lea, 1838); M. (Aph.) za- 
letus (Binney, 1837). 

Subgenus Mesodon (Akromesodon) 
Emberton, 1991 

Type species: Polygyra andrewsae norma- 
lis Pilsbry, 1900, by ohginal designation. 

Definition: The first Mesodon to possess 
characters #112 and 113, and all of its de- 
scendents. 

Species: M. (Akr.) altivagus (Pilsbry, 1990); 
M. (Akr.) andrewsae Binney, 1879; M. (Akr.) 
normalis (Pilsbry, 1900). 

Subgenus Mesodon (Mesodon) s.s. 

Definition: The first Mesodon to possess 
characters #114 and 115, and all of its de- 
scendents. 

Species: M. (M.) clausus (Say, 1821); M. 
(M.) sanus (Clench & Archer, 1933); M. (M.) 
thyroidus (Say, 1817); M. (M.) trossulus Hu- 
bricht, 1966. 

Shell-Based Phylogenetic Analysis 

Figures 9-1 1 present x-ray outlines of 57 
shells representing polygyrid subgenera and 
outgroups. These outlines were used for phy- 
logenetic character analysis. Also included in 
the character analysis were the x-rayed 



shells themselves, plus four shells from the 
ANSP collection representing four additional 
species: Ashmunella angulata, Stenotrema 
(Archerelix) barbigerum, S. (Pilsbrelix) ex- 
odon, and S. (Toxotrema) hirsutum. No shell 
was available of Hochbergellus hirsutus, but 
its published description (Roth & Miller, 1992) 
was used to score as many characters as 
possible. Thus, a total of 62 species were 
included, of which only five lacked x-ray 
data. 

Table 2 defines the 14 characters and 71 
character states scored for phylogenetic 
analysis, which are illustrated in Figures 12, 
13, and 6. All of these characters and char- 
acters states are new or newly evaluated. 

Figure 14 shows the distributions of shell 
characters among subgenera and species. 
Figure 15 diagrams shell characters that 
were excluded from phylogenetic analysis 
because of known high levels of homoplasy 
within subgenera of the Triodopsini and Me- 
sodontini. 

Figure 16 shows the results of cladistic 
analysis of the data in Figure 14. In total, 
Hennig86 generated 1,529+ equally and 
maximally parsimonious cladograms with a 
consistency index of 0.34 and a retention in- 
dex of 0.68, of which Figure 16 is the Nelson 
consensus tree. 

Reliability of Fossils 

Comparison of shell-based and anatomy- 
behavior-shell-based phylogenetic hypothe- 
ses revealed conspicuous differences in res- 
olution and topology. Among 54 ingroup 
(polygyrid) taxa, with a maximum possible 
resolution of 53 nodes, the shell hypothesis 
(Fig. 16) had 10 nodes (19% of maximum) 
and the anatomy-behavior-shell hypothesis 
(Fig. 8) had 40 nodes (75% of maximum). 
Thus, the anatomy-behavior-shell hypothesis 
had four times the resolution of the shell- 
based hypothesis. 

Topologically, the only congruence be- 
tween the two hypotheses was in the 
Stenotremini, which both showed as a mono- 
phyletic clade with Euchemotrema and 
Stenotrema (Cohutta) at its base. Other 
clades showed major discrepancies between 
the two phylogenetic hypotheses. Thus, rel- 
ative to the anatomy-behavior-shell hypoth- 
esis/revision, the shell-based hypothesis (a) 
grouped Vespericola and Appalachina, Dae- 
dalocheila (Upsilodon) hippocrepis and Lo- 
bosculum, and Polygyra and Millerelix (Prat- 



94 



AIA 





EMBERTON 
AID 




CB 




CM 






App 




DUa 





Lnb 











FIG. 9. 



FIGS. 9-11. Shell ontogenies, from x-rays of adult shells, of representatives of polygyria subgenera and of 
polygyhd closest outgroup families. The representatives are type species unless otherwise indicated. All 
scale bars = 3 mm. The shells are arranged by a previous classification (Webb, 1974; Richardson, 1986), 
since revised (Emberton, 1994a, this paper). Dotted lines indicate portions of the x-rays that were difficult 
to interpret. By chance the x-rayed shell representing Ashmunella (As) was broken internally; all characters 
could be scored from this drawing, however, so the specimen was not replaced. Specimen abbreviations, 
defined in alphabetical order with their catalog numbers at the Academy of Natural Sciences of Philadel- 
phia, are: AIA, Mogona (Mogona) profunda, 77867; AID, Mogona (Dysemdoma) townsendiana, 1 00390; 
App, Appalachina sayana, 139140; As, Ashmunella rhyssa, 166077; CB, Cryptomastix (Bupiogona) hend- 
ersoni, 171267; CO, Cryptomastix (Cryptomastix) mullani, 171245; CM, Cryptomastix (Micranepsia) ger- 
mana, 1 1 154; DD, Daedalochila (Daedalocheila) auriculata, 57070; DU, Daedalochila (Upsilodon) liippocre- 
pis, 84629; DUa, D. (U.) acutidentata, 166418; E, Eucliemotrema leal, 172539; F, Fumonelix wheatleyi, 
169691; G, Giffordius pinclioti, 150735; IH, Inflectarius (Hubrichtius) downieanus (non-type), 91035; II, 
Inflectarius (Inflectarius) inflectus, 91616; llf, /. (I.) ferrissi, 98085; Lb, Lobosculum pústula, 86968; Ln, Linisa 
anilis, 166371; Lnb, Linisa behri, 166487; MeA, Mesodon (Aphalogona) elevatus, 81161; MeK, Mesodon 
(Akromesodon) normalis, 169640; MeM, Mesodon (Mesodon) thyroidus, 71950; MiM, Millerelix (Millerelix) 
mooreana, 158375; MiP, Millerelix (Prattelix) plicata, 143448; NA, Neofielix (Asamiorbis) dentifera, 78876; 



(continued) 



POLYGYRID SHELL EVOLUTION 





Po 




PrE 



PrF 




PrX 




PrP 




SSp 





SSm 





FIG. 10. 




NN, Neohelix (Neohelix) albolabhs, 75843; NS, Neohelix (Solemorbis) solemi, 182281 ; OB, outgroup Brady- 
baenidae: Bradybaena similahs, 174469; ОС, outgroup Camaenidae Pleurodonte lynchnuchus, 32588; OH 
outgroup Helminthoglyptidae: Helminthoglypta tudiculata. 112911; OS, outgroup Sagdidae; Sagda cooki- 
ana, 139388; ОТ, outgroup Thysanophoridae; Thysanophora impura, 177310; OX, outgroup Xanthony- 
chidae; Cepolis cepa, 33301; PaP, Patera (Patera) appressa, 335137; PaR, Patera (Ragsdaleorbis) penn- 
sylvanica, 251512; PaV, Patera (Vesperpatera) binneyana, 176765; Po, Polygyra septemvolva, 69117; PrE, 
Praticolella (Eduardus) martensiana, 98578; PrF, Praticolella (Farragutia) mobiliana, 105999; PrP, Praticolella 
(Praticolella) ampia, 131749; PrX, Praticolella (Filapex) jejuna, 77035; SO, Stenotrema (Cohutta) cohuttensis, 
170118; SS, Stenotrema (Stenotrema) stenotrema, 169148; SSm, S. (S.) maxillatum, 170141; SSp, S. (S.) 
spinosum, 11383; ST, Stenotrema (Toxotrema) hirsutum, 11396; Tb, Trilobopsis loricata, 11149; TdB, 
Triodopsis (Brooksorbis) platysayoides, 183201; TdH, Triodopsis (Haroldorbis) cragini, 186723; TdM, Th- 
odopsis (Macmillanorbis) rugosa, 174909; TdP, Triodopsis (Pilsbryorbis) tennesseensis, 139143; TdS, Tri- 
odopsis (Shelfordorbis) vulgata, 68807; TdT, Triodopsis (Triodopsis) tridentata, 211921; TdV, Triodopsis 
(Vagvolgyorbis) juxtidens, 64720; V, Vespericola Columbians, 158355; W, Webbhelix multilineata, 190168; 
XW, Xolotrema (Wilcoxorbis) fosteri, 157255; XX, Xolotrema (Xolotrema) denotata, 128444. 



96 




EMBERTON 
TdB 



TdM 




TdP 



TdS 




TdT 



TdV 










FIG. 11 



telix), each pair of which has been classified 
into two widely separated clades; and (b) 
split Ashmunella rhyssa and A. angulata, 
Daedalocheila (Upsilodon) hippocrepis and 
D. (U.) acutidentata, Praticolella and Lobos- 
culum, Linisa anilis and Linisa behri, Millerelix 
(Millerelix) and M. (Prattelix), and Polygyra 
and Giffordius, each pair of which has been 
classified into a single, closely related clade. 
Among outgroups, the shell-based hypothe- 
sis conflicted with a previous, anatomy- 
based hypothesis (Emberton, 1991c; Fig. 8) 



by joining Cepolis In a clade with Pleurodonte 
and Sagda. 



Closest Convergences in Sympatry 

Figure 1 shows the closest known, field- 
validated, polygyrid convergences in sympa- 
try on the globose, umbilicate, flat, and tri- 
dentate shell forms. As mentioned in the 
Introduction, the globose case is the closest 
convergence and has received detailed 



POLYGYRID SHELL EVOLUTION 



97 



TABLE 2. Shell characters used for a separate phylogenetic analysis of the Polygyridae (Fig. 16). 

1 . Shape of the aperture's generating curve throughout late-juvenile ontogeny (Fig. 12: 1 ). 1a, 
"egg," "pinto bean," or "lima bean." lb, "kidney bean." 1c, "bulging kidney bean." 

2. Approximate number of complete adult whorls (Fig. 12; 2, which shows the shell apex 
down). 2a, four. 2b, five. 2c, six. 2d, eight. 2e, nine. 

3. Approximate ratio of apertural areas three whorls apart, beginning near the apex and 
ending at least 3/4-whorl before the aperture (Fig. 12: 3). 3a, 40:1. 3b, 32:1. 3c, 15:1. 3d, 
9:1. 3e, 7:1. 

4. Golumellar surface of the body whorl approximately 1/4-whorl before the adult aperture 
(Fig. 12: 4). 4a, flat or slightly concave, but convex at the suture. 4b, flat or slightly concave, 
flat at the suture. 4c, convex throughout. 

5. Umbilical shape (Fig. 12: 5, which outlines the x-rayed umbilici). 5a-5h, extremely narrow 
to broad (some intergradation among categories). 

6. Umbilical sutures (Fig. 13: 6). 6a, strongly to weakly shouldered. 6b, rounded, unshoul- 
dered. 

7. Umbilical-wall whorls (Fig. 13: 7). 7a, flat. 7b, slightly flat. 7c, round. 

8. Basal denticle(s) (Fig. 13: 8). 8a, absent. 8b, baso-columellar shoulder or knob parallel to 
apertural plane. 8c, partial lamella parallel to apertural plane. 8d, basal denticle parallel to 
apertural plane. 8e, denticle or lamella(e) transverse to apertural plane. 8f (= Fig. 6: char- 
acter 4), complete lamella parallel to apertural plane. 

9. Parietal denticle shape (size variable) (Fig. 13: 9). 9a, absent. 9b, linear, curved toward the 
umbilicus, higher toward the aperture. 9c (= Fig. 6: character 5), linear, straight, even in 
height. 9d (= Fig. 6: character 6), Triangular to spatulate. 9e, linear, curved away from the 
umbilicus, higher away from the aperture. 

10. Size (Fig. 13: 10). lOa-IOi, gigantic to minute (some intergradation among categories). 

1 1 . Gradually increasing outward tilt of the long axis of the aperture (= Fig. 6: character 1 ). 1 1 a, 
throughout ontogeny or until tilting upward slightly. 1 1 b, until tilting upward conspicuously. 

12. Whorl expansion rate (= Fig. 6: character 2). 12a, constant. 12b, increasing then decreas- 
ing, with successive whorls always larger. 12c, increasing then decreasing, such that 
successive whorls are equal. 

13. Lower apertural lip (= Fig. 6: character 3). 13a, separate from basal shell. 13b, joined to 
basal shell as a thin callus. 

1 4. Palatal denticle (= Fig. 6: character 7). 1 4a, absent. 1 4b, discrete, parallel to apertural plane. 
14c, non-discrete, forming a thin shelf grading into the basal denticle, parallel to apertural 
plane. 14d, semidiscrete, with bottom tapering and thinning, basally slanted inward into the 
apertural plane. 



study, including discoveries of several sites 
of sympatry (Emberton, 1994b, 1995b). 

The second closest shell-form conver- 
gence in sympatry is on the flat form, exhib- 
ited by the mesodontin Patera (Patera) laevior 
and the triodopsin Xolotrema (Wilcoxorbis) 
fosteri. Fieldwork in April 1981 along the 
lower Ohio River Valley, visiting all stone 
bluffs reasonably accessible by road, accu- 
mulated collections at 22 stations (numbered 
as "H-1" through "H-22"), all material from 
which is catalogued at the Field Museum of 
Natural History. Both species had been re- 
ported from Grand Chain, Indiana (Pilsbry, 
1940), but extensive search failed to find both 
in 1981, perhaps due to recent floods. Sym- 
patry between P. laevior and X. fosteri was 
discovered at only one station: on a sand- 



stone wall above the Ohio River at the Fern 
Cliff estate, Hawesville, Hancock County, 
Kentucky, 21 April 1981. 

Figure 17 illustrates the external anato- 
mies, shells, and dissected reproductive 
anatomies of representative specimens of 
Patera laevior and Xolotrema fosteri from the 
Hawesville, Kentucky, site, and summarizes 
their mating-behavioral differences accord- 
ing to Webb (cited in Emberton, 1994a). The 
shells and external bodies were virtually iden- 
tical in size and shape (Figs. 1, 17), but inter- 
nally X. fosteri differed from P. laevior by its 
penial sheath, penial retentor muscle, retrac- 
tor-muscle attachment on the vas deferens, 
and thick gametolytic-gland (= spermathecal) 
duct, all correlating with its internal (vs. 
external) sperm exchange (Fig. 17). Ecologi- 



98 



EMBERTON 












Ь 






\^ } I^ ß Л n л л 

а b с d е f g' ' h 

FIGS. 12-13. Shell characters among polygyhd subgenera, in addition to those in Fig. 6. Definitions are 
given in Table 2. 



6 <— - 



POLYGYRID SHELL EVOLUTION 

a 



99 




8 



^ 
^ .* 



^4^ 








3 




10mm 



FIG. 13. 



cal and conchological data on the two sym- 
patrlc populations (Emberton, unpublished) 
are archived at the Academy of Natural Sci- 
ences of Philadelphia. 

The third closest shell-form convergence in 
sympatry is on the umbilicate form, exhibited 
by the mesodontin Appalachina sayana and 
the allogonin Allogona (Allogona) profunda. In 
the northern Midwest, these species' ranges 
overlap extensively (Hubricht, 1985), but ex- 
amination of Field Museum collections indi- 



cated only a few cases of documented sym- 
patry, of which the most conchologically 
similar case was at Burnside, Pulaski County, 
Kentucky (Fig. 1). Extensive search of that 
region in spring of 1982 failed to yield both 
species, perhaps due to degradation of rem- 
nant forest. Sympatry was discovered, how- 
ever, at a site on the northern slope of Pine 
Mountain, Harlan County, Kentucky (station 
"GS-1 1 6"). At that site, the shell convergence 
was not as extreme as in Figure 1 , because 



100 



EMBERTON 



т^ 



OB 

ox 
он 
от 

ОС 

s 



-W 

-NN 

-NS 

-NA 

-XW 

-XX 

-TdS 

-TdB 

-TdP 

-TdM 

-TdH 

-TdT 

-TdV 



1 — V 



I г 



ce 

CM 
Tb 
Al A 
AID 



-E 

-SC 

-SA 

-SP 

-SS 

-SSp 

-SSm 

-ST 



_ L 



Ul- 



po 

Ln 

Lnb 

Lb 

PrF 

PrE 

PrX 

PrP 



-p-MlM 
l— MiP 
DU 



€ 



DUa 
DD 



t: 



r 



€i 



PaV 

PaR 

Pap 

IH 

II 

Ilf 

F 

App 

MeA 

MeK 

MeM 



-Asa ? 
-Asr a 



4 5 

с b 

b с 

с b 

с h 

b d 

b a 



8 1 

a a 

e a 

a a 

a a 

e a 

e a 



10 11 
e a 



12 13 14 

a a a 

a a a 

a a a 

a a a 

a a a 

a a a 



с с 

a с 

a с 

a с 

с в 

а в 

с h 

с f 

с в 

с в 

с g 

с в 

с в 



а а 

b а 

b а 

с Ь 

с Ь 

с b 

d b 

с b 

d b 

d b 

d b 

d b 

d b 



a a a 

a a a 

a a a 

a a a 

a a b 

a a b 

a a b 

a a a 

a a b 

a a b 

a a b 

a a b 

a a b 



b b 
b a 



с e 

с d 

a с 

a e 

с d 

с с 



a с 

a с 

a с 

a с 

a с 

a b 



b b 

с b 

b b 

d b 

b a 

b a 



a a a 

a a a 

a a a 

a a b 

a a a 

a a a 



e e 
b b 



b 9 

b d 



с g 

с e 



a с 
a с 



b с 
с с 
b d 



a d 

с f 

с d 

9 •? 



f С 

f С 

f с 

f с 

£ с 

f с 

f с 

f с 



a a 

с a 

с b 

a a 

d b 

с b 

a b 

e b 

с b 

b a 

b b_ 



a a a 

a a a 

a a a 

a a a 

a a b 

a a a 

a a a 

a a a 

a a a 

a a a 

a a a 



FIG. 14. Distributions of shell characters among polygyria subgenera. Characters are numbered as in Table 
2, but character-states are converted to letters (a = 1, b = 2, etc.). 



POLYGYRID SHELL EVOLUTION 



101 



rr^ 






FIG. 15. Shell variation discounted as characters: a, low-to-high spires are documented within Patera s.S.; 

b, rounded-to-angulate-to-keeled peripheries occur within Xolotrema s.S., X. (Wilcoxorbis), and Patera s.S.; 

c, covered-to-open umbilici are known within both Patera (Vesperpatera) and Mesodon s.S.; d, smooth- 
to-ribbed sculpture appears within Xolotrema s.S., Triodopsis s.S., T. (Pilsbryorbis), and T. (Haroldorbis); e, 
bald-to-hirsute sculpture occurs within Xolotrema s.S., Inflectarius (Summinflectarius), and Fumonelix; f, 
unicolor-to-color-banded shells are known within both Mesodon s.s. and M. (Aphalogona). 



App. sayana tended to have a smaller shell 
than AI. profunda. The northern Midwest was 
not extensively surveyed during 1982 and 
1983 fieldwork, however, so closer conver- 
gences in sympatry on the umbilicate shell 
form may exist in that region. 

Least close — but still remarkable, espe- 



cially in apertural-barrier construction — of the 
four polygyrid shell-form convergences in 
sympatry (Fig. 1) is on the tridentate form. 
The closest field-documented case of triden- 
tate convergence in sympatry comprises the 
mesodontin Inflectarius (Inflectarius) inflectus 
and the triodopsin Triodopsis (Triodopsis) fal- 



102 



EMBERTON 



OB 
=PrP 

=он 
=от 
=ох 
=ос 



юз 



=NN 

=NS 

=NA 

=XW 

=XX 

=TdS 

=TdB 

=TdP 

=TdM 

=TdH 

=TdT 



=TdV 

=H 

=V 

=App 

=CB 

=CC 

=CM 

=Tb 

=А1Л 

=A1D 

=Asr 

=E 

=SC 

=SA 

=SP 

=SS 

=SSp 

=SSm 

=ST 



=Ln 
=PrF 
=PrE 
=PrX 
=DU 
=Lb 
=MiM 
=Asa 
=Lnb 
=DUa 
=DD 
=Po 
=MiP 
=PaV 
=PaR 
=PaP 
=IH 
=11 
=IIf 
=F 

=MeA 
=MeK 
=MeM 



FIG. 16. Shell-based consensus tree of poiygyrid subgenera resulting from cladistic analysis of data in Fig. 

14. 



POLYGYRID SHELL EVOLUTION 



103 




Lengthy courtship and nnating 

Intertwining of penes 

External deposition of sperm 
nriass on nnate's everted penis 





Brief courtship and nnating 

Insertion of penes 

Internal deposition of sperm 
mass in spermathecal duct 





FIG. 1 7. Closest known convergence in sympatry on the flat shell form: Patera laevior (left) and Xolotrema 
fosteri (right) from Hawesville, Hancock County, Kentucky. Center: external anatomies and shells in two 
views. Bottom: dissected reproductive anatomies. Sides: mating-behavioral differences according to Webb 
(cited in Emberton, 1994a). 



lax, v^hich I collected together under the 
same log in dense woods, Vinton County, 
Ohio, in 1979 (vouchers at Field Museum of 
Natural History, Chicago). The ranges of 
these tv^o species overlap moderately in the 
central Midwest, and other cases of sympa- 
try are documented — sometimes as inadvert- 
ently mixed lots — in the collection of the 
Academy of Natural Sciences of Philadelphia 
(Emberton, unpublished). 



Shell Barriers and Water Loss 

Table 3 gives the results of the experiment 
on Triodopsis tridentata. A total of 280 "snail- 
hours" were recorded. Snails from which ap- 
ertural barriers had been removed lost water 
by evaporation faster than those with barriers 
left intact: 27% faster when inactive (re- 
tracted into the shell) and 9% faster when 
active (extended from shell). 



104 



EMBERTON 



Snails with intact barriers were 83% more 
successful than those from which barriers 
had been removed in forming complete or 
partial epiphragms. Epiphragms slightly re- 
duced the rate of evaporative water loss in 
snails with barriers intact (by 3% for both 
partial and complete epiphragms). In snails 
from which barriers had been removed, how- 
ever, epiphragms greatly reduced the rate of 
water loss: by 22% for partial epiphragms 
and by 38% for complete epiphragms. 

Remaining Conservation Priorities 

Table 4 gives highest priorities for polygy- 
rid conservation for each of four, phylogeny- 
based categories. In the category of radiat- 
ing, endemic clades, Fumonelix must rank 
very high; the genus is restricted to the 
southern Appalachians, and three of its six 
species are narrow-range endemics that 
have been officially designated as endan- 
gered or threatened: F. archeri, F. jonesianus, 
and F. orestes. In the same category, al- 
though Mesodon (Akromesodon) contains 
the widespread and relatively common spe- 
cies M. normalis, its other two species both 
have narrow, high-altitude ranges: M. altiva- 
gus on summits of the Great Smoky Moun- 
tains, and M. andrewsae on the summit of 
Mount Rogers, Virginia. 

Four species have been listed as high pri- 
orities for conservation in the category of ex- 
tremely autapomorphic endemics. The two- 
species genus Giffordius, endemic to 
Colombia's tiny Isla de Providencia (off the 
eastern coast of Nicaragua), is unique within 
the family for its ovoviviparity; Giffordius pin- 
choti by far is the rarer and most endangered 
of the two species (Emberton, unpublished). 
Inflectahus ferrissi, endemic to high eleva- 
tions of the Smoky Mountains, represents 



extreme phylogenetic shifts in both shell 
morphology (Emberton, 1 991 a, 1 991 b) and in 
penial morphology (Emberton, 1991a). Triod- 
opsis platysayoides, endemic to a few bluffs 
along the New River Gorge of northeastern 
West Virginia, U.S.A., also embodies extreme 
phylogenetic divergences in both shell and 
penis (Emberton, 1988a). Mesodon chilhow- 
eensis is remarkable for its gigantic, broadly 
umbilicate shell, exhibiting nearly regular, 
log-spiral growth (Emberton, 1994a: fig. 1) 
and for its extremely long penis, much longer 
than the diameter of the shell (Emberton, 
1991a). 

Giffordius also deserves high priority for 
conservation in another category, as relic sis- 
ter-group to a major clade. According to the 
general phylgenetic hypothesis (Fig. 8), Gif- 
fordius is basal to the Polygyrini, hence is 
sister-group to the remaining Polygyrini, a 
highly diverse and speciose clade. 

The conservation category of localities 
with diverse sympatric convergences is led 
by the northern slope of Pine Mountain, Har- 
lan County, Kentucky. This is the only known 
site where convergences on all four polygyrid 
shell forms (Fig. 1) coexist. There the globose 
form is represented by Mesodon zaietus and 
Neotielix albolabris; the umbilicate form by 
Appaiactiina sayana and Allogona profunda 
(mentioned above); the flat form by Patera 
appressa and Xolotrema denotata; and the 
tridentate form by Inflectahus inflectus, Tri- 
odopsis vulgata, and T. tridentata (Emberton, 
1995c). This site is also important as North 
America's most diverse known locality for 
land snails (Emberton, 1995c). 

Thus, Table 4 lists seven high priorities (in- 
cluding a double listing of Giffordius) for poly- 
gyrid conservation, based on phylogenetic 
criteria. Five of these priorities are currently 
under protection. The Smoky Mountains are a 



TABLE 3. Effect of apertural dentition and epiphragm on the rate of 
evaporative water loss in Triodopsis tridentata. 



Category 



Number of 
'Snail-Hours' 



Mean Rate of 
Water Loss 



Toothed, no epiphragm 
Toothed, partial epiphragm 
Toothed, complete epiphragm 
Toothless, no epiphragm 
Toothless, partial epiphragm 
Toothless, complete epiphragm 
Toothed, after activity 
Toothless, after activity 
Total "Snail-Hours" 



70 


3.86% 


59 


3.74% 


26 


3.73% 


63 


4.90% 


7 


3.97% 


20 


3.06% 


25 


15.80% 


10 


17.18% 


280 





POLYGYRID SHELL EVOLUTION 105 

TABLE 4. Conservation high priorities for polygyrids, based on four phylogenetic criteria. 



Criterion 



High Priority 



#Spp 



Locality 



Protected? 



Radiating, endemic clade Fumonelix 6 Southern Blue Ridge, U.S. A 

Radiating, endemic clade Mesodon (Akromesodon) 3 Southern Blue Ridge, U.S. A 
Extremely autapomorphic 

endemic Giffordius pinchoti 

Extremely autapomorphic 

endemic Inflectarius ferrissi 

Extremely autapomorphic 

endemic Triodopsis platysayoides 

Extremely autapomorphic Mesodon 

endemic chilhoweensis 

Relic sister-group to 

major clade Giffordius 

Diverse sympatric four shell-form 

convergences convergences 



1 Isla de Providencia, Colombia 

1 High Smoky Mountains, U.S.A. 

1 New River Gorge, U.S.A. 

1 Smoky Mountains, U.S.A. 

2 Isla de Providencia, Colombia 
11 Pine Mountain, Kentucky, U.S.A. 



Yes 
Yes 

No 

Yes 

Yes 

Yes 

No 

No 



U.S. National Park and International Bio- 
sphere Reserve, protecting four species of 
Fumonelix, two species oí Mesodon (Akrome- 
sodon), Inflectarius ferrissi, and Mesodon 
chilhoweensis. The remaining Fumonelix are 
protected in U.S. National Forests, and the 
remaining M. (Akromesodon) is protected by 
Mount Rogers State Park. Tnodopsis 
platysayoides is somewhat protected in Coo- 
pers Rock State Forest, West Virginia, U.S.A. 

Two high-priority sites remain unprotected. 
There is a "Pine Mountain State Park," Bell 
County, Kentucky, but it is about 64 km away 
from and has a much lower diversity than the 
Harlan-County Pine Mountain site listed in Ta- 
ble 4 (Emberton & Petranka, unpublished). 
Thus, the Pine Mountain site, U.S.A., is un- 
protected. 

Also unprotected is the conservationally 
important, small Isla de Providencia, Colom- 
bia. In 1987, both species of Giffordius were 
still surviving on the island in remnant 
patches of forest, primarily at higher eleva- 
tions, but deforestation had already de- 
stroyed the type locality of G. pinchoti and 
seemed to be rapidly advancing up the cen- 
tral peak (Emberton, 1992, unpublished). 



DISCUSSION 

General Phylogenetic Hypothesis/Revision 

This hypothesis/revision culminates the 
author's 15 years of work on polygyrid sys- 
tematics, and hopefully provides a replicable 
data set and a fully testable hypothesis upon 
which future workers may build. For allozyme 



data and for more detailed phylogenetic hy- 
potheses on the Triodopsini and the Meso- 
dontini, see Emberton (1988a, 1991a, 1994). 
For a polygyrid biogeographic/historical hy- 
pothesis, see Emberton (1994a). Clearly, this 
is not the final word; much remains to be 
learned. 

Shell-Based Phylogenetic 
Analysis/Reliability of Fossils 

Despite the discovery of many new char- 
acters, shell-based phylogenetic analysis re- 
sulted in very low resolution. Two possible 
sources of additional shell characters were 
neglected, however: shell-surface micro- 
sculpture (Emberton, 1995b) and shell ultra- 
structural layers (Boggild, 1930; Wilbur & 
Saleuddin, 1983; Roth, 1987; Watabe, 1988). 
Both of these should be investigated. Quali- 
tative character analysis of x-ray data failed 
to detect a difference in whorl expansion rate 
between the Triodopsini and the Mesodontini 
suggested by quantitative analysis (Ember- 
ton, 1994a). Thus, more subtle analysis of 
x-rays could yield more characters for phylo- 
genetic resolution. Based on current data, 
however, "shells do not tell" the estimated 
145 million years of phylogenetic history of 
the Polygyridae in North America (Emberton, 
1994a). This implies that identification of pre- 
Miocene polygyrid fossils may be very diffi- 
cult at best. 

Thus, based on the general phylogenetic 
hypothesis/revision, convergences in shell 
morphology were rampant within the Poly- 
gyridae. "Kidney-bean" generating curves 
cropped up in one subgenus each of Poly- 



106 



EMBERTON 



дуга and Daedalochila. Whorl-counts of 
over six hypothetically evolved one or nnore 
times each in the Triodopsini, Vespericolini, 
Stenotremini, Polygyrini, and Mesodontini. 
Extremely \o\n whorl-expansion rates (< 2.7 
per 360-degree rotation) seemingly evolved 
independently in the Triodopsini, Stenotrem- 
ini, and Polygyrini. Convergences on a col- 
umellarly flattened body whorl seem to have 
occurred in all polygyrid tribes except the 
Ashmunellini. Expanded umbilici (Fig. 12: 
char 5e-g) appeared in all tribes but the Ves- 
pericolini. Rounded, unshouldered umbilical 
sutures seems to be a good synapomorphy 
of the genus Triodopsis, but nevertheless this 
character-state was apparently reversed in 
the nominal subgenus and seems to have 
been converged upon in the outgroup family 
Camaenidae. Slightly flattened umbilical-wall 
whorls seemingly arose convergently within 
one or more subgenera each of the Triod- 
opsini, Allogonini, and Mesodontini. Although 
transverse-to-spiral basal lamellae in Ash- 
munella, Daedalochila, and Appalachina were 
hypothetically plesiomorphic and hence not 
necessarily convergent, all other forms of 
basal denticles and lamellae seem to have 
been converged upon repeatedly in the Poly- 
gyridae, with the single exception of the com- 
plete basal lamella, which is a hypothetical 
synapomorphy of the Stenotremini. Two 
types of parietal denticles — straight and tri- 
angular-to-spatulate — seem to be good syn- 
apomorphies, with additional phylogenetic 
information, for the Stenotremini and the 
Polygyrini, although the latter was apparently 
lost secondarily in Practicolella; a down- 
curved parietal denticle, however, seems to 
have evolved independently in all other tribes 
of the Polygyridae (non-type species of Ves- 
pericola also have it: Pilsbry, 1940). Both ex- 
tremes of shell size occur among the out- 
groups, and various intermediate and small 
sizes recur repeatedly among polygyrid sub- 
genera, with only very slight tendencies to- 
ward trends within and among tribes. Rapid 
shifts in apertural tilt and expansion rate are 
apparent synapomorphies for a subset of the 
Polygyrini, yet both were hypothetically re- 
versed in type species of some genera. An 
adnate, callus-like apertural basal lip may 
seem a perfect synapomorphy for four of 
Stenotrema's five subgenera, but was appar- 
ently reversed in S. (Archerelix) barbigerum 
(Pilsbry, 1940). Regarding apertural palatal 
denticles, discrete denticles (apertural barri- 
ers) seem to appear sporadically in nearly all 



polygyrid tribes; and semidiscrete, basally 
recessed denticles seem to be only an incon- 
sistent synapomorphy of the Polygyrini; but a 
non-discrete "shelf" seems to be a good sy- 
napomorphy of the Stenotremini. 

Closest Convergences in Sympatry 

Identifications and field verifications of the 
closest convergences in sympatry on the flat, 
umbilicate, and tridentate polygyrid iterated 
shell forms (Fig. 1) provide starting points for 
analyses of these naturally replicated exper- 
iments in evolutionary morphology, such as 
those already conducted on the globose shell 
form (Emberton, 1994b, 1995a). Although 
these four cases of polygyrid shell conver- 
gence in sympatry (Fig. 1; Emberton, 1994a) 
are the most precise known in North Amer- 
ica, they are representative of numerous less 
precise cases involving the same four basic 
shell forms. Among and within these four 
shell forms, there are other examples of con- 
vergence (Emberton, 1988a, 1991a, 1994a), 
the most striking (and informative for polygy- 
rid evolution) of which is between Inflectarius 
ferrissi and Neohelix dentifera (Emberton, 
1991b). 

Shell Barriers and Water Loss 

The experimental results from Triodopsis 
tridentata suggest that apertural barriers re- 
duce the rate of evaporative water loss both 
directly and indirectly, by aiding in the forma- 
tion of an epiphragm. The manner in which 
barriers and epiphragms retard water loss 
may be counter-intuitive, judging from Ram- 
say's (1935) experiments on evaporation 
rates from vertical tubes. Ramsay observed 
faster water loss when the evaporating sur- 
face was at the bottom of the tube than at the 
top, but found that the presence of a perme- 
able occluder tended to diminish the differ- 
ence. He hypothesized therefore that "when 
[the evaporating surface] is at the bottom . . . 
there is an upward current of moist air which 
sets up a circulation in the system." Ram- 
say's hypothesis has not been tested, to my 
knowledge. Extending his hypothesis to land 
snails, when a snail withdraws deeply (to es- 
cape prédation, for example) into the coiled 
tube of its shell, its apertural barriers (and the 
epiphragm they aid in forming) may function 
not so much to physically block diffusing wa- 
ter vapor as to interrupt the convection cur- 



POLYGYRID SHELL EVOLUTION 



107 



rents that normally result from tubular evap- 
oration. 

The trend for apertural barriers in T. triden- 
tata and other triodopsins to be larger in 
moister habitats (Emberton, 1988a) suggests 
that their demonstrated retardation of evap- 
orative water loss is not their only — or even 
primary — function. Other hypothesized func- 
tions are given in the Introduction. 

Polygyhds provide some fascinating ex- 
amples of apertural obstruction that could be 
used to test these and other hypotheses. Fig- 
ure 2 presents some extreme examples from 
several clades, most of which have arisen by 
evolutionary convergence. The most extreme 
cases are in the genus Stenotrema; it is a 
memorable experience to watch one of these 
snails extend, its body "pouring" like molas- 
ses through the slit-like, convoluted aperture. 
This slit seems to be at its most narrow in S. 
(Pilsbrelix) uncifera, but is augmented in S. 
(Stenotrema) maxHlatum (both in Fig. 2) by 
recession of the basal lamella, which lacks a 
notch and which is overlapped by the parietal 
lamella to form a three-dimensional baffle. 

Species of Daedalochila have some com- 
plex apertural conformations, the most bi- 
zarre of which are the deeply recessed pari- 
etal scoop in D. (Upsilodon) hippocrepis and 
the convoluted apertural lip incorporating the 
parietal scoop and augmented by recessed 
denticles in D. (Daedalochila) uvullfera (both 
in Fig. 2). Other notable examples occur in 
Triodopsis, Lobosculum, Ashmunella, LInlsa, 
Lobosculum, and Inflectahus (some are illus- 
trated in Figs. 1 and 2). 

Remaining Conservation Priorities 

The evaluation of conservation priorities 
presented in this paper is doubtless biased 
by the author's limited experience with the 
western and subtropical species. Table 4 is 
intended only as a preliminary guideline and 
as a possible format for future, more enlight- 
ened assessments. 

Given these caveats. Table 4 suggests that 
most phylogenetically important polygyrids 
are reasonably well protected against extinc- 
tion due to habitat loss. How well they and 
other polygyria species will withstand envi- 
ronmental degradation due to acid rain 
(Graveland et al., 1994), local extinctions of 
forest-canopy tree species (Getz & Uetz, 
1994), and global warming, remain to be dis- 
covered, however. Unfortunately, there is no 
long-term monitoring study being conducted 



on any polygyrid population or community, to 
my knowledge. 

Two remaining conservation priorities do 
demand rapid attention, however: Isla de 
Providencia, Colombia, and Pine Mountain, 
Harlan County, Kentucky, U.S.A. (Table 4). 
The high conservation importance of these 
sites almost assuredly applies to many other, 
lesser-known, leaf-litter/soil invertebrates 
that polygyrids represent. 



ACKNOWLEDGEMENTS 

Supported in part by National Science 
Foundation grants BSR-8700198 and DEB- 
9201060 and by Academy of Natural Sci- 
ences of Philadelphia (ANSP) discretionary 
funds. I am also grateful to S. Schaefer and 
G. Böhlke for access to the x-ray facility. Ich- 
thyology Department, ANSP; to E. Gitten- 
berger for steering me to the Chhstelow and 
Falkner papers; and especially to T. Pearce, 
B. Roth, and an anonymous reviewer for very 
useful comments on a previous draft of the 
manuscript. I would like to take this opportu- 
nity to thank fellow polygyrid workers who 
have generously helped me with this and 
other projects during the past 15 years: T. 
Asami, K. Auffenburg, N. Babrakzai, A. 
Bogan, J. Burch, R. Caldwell, H. L. Fair- 
banks, H. Feinberg, H. В. Foster, R. Fulling- 
ton, G. Goodfriend, F. W. Grimm, L. Hubricht, 
E. Keferl, G. Long, С Mather, R. Maze, G. 
McCracken, W. Miller, J. Murray, R. Neck, T. 
Pearce, J. Petranka, W. Pratt, R. Reeder, В. 
Roth, R. Seiander, the late A. Solem, A. 
Stiven, R. Taylor, F. Thompson, J. Vagvolgyi, 
A. Van Devender, W. Van Devender, and G. 
Webb. 



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Revised MS. accepted 10 January 1995 



MAUXCOLOGIA, 1995, 37(1): 111-122 

GEOGRAPHIC DISTRIBUTION AND SHELL COLOUR AND BANDING 

POLYMORPHISM IN MARGINAL POPULATIONS OF CEPAEA NEMORALIS 

(GASTROPODA, HELICIDAE) 

A. Honèk 

Department of Entomology, Research Institute of Plant Production, Ruzyné 507, 161 06 

Praha 6, Czech Republic 

ABSTRACT 

Occurrence and colour and shell banding polymorphism were investigated in populations of 
Cepaea nemoralis (L.) at the edge of the species' geographic distribution in the Czech Re- 
public. Cepaea nemoralis populations were found only at intravillan localities. The great majority 
of town and village localities were occupied by С nemoralis in three isolated areas: a northern 
one integrated with the main geographic area of the species, and two isolated southern insular 
areas. A few populations were scattered at localities between these areas and further south, 
where C. nemoralis was replaced by Cepaea hortensis (Müller). The С nemoralis distribution 
area and abundance may have increased since 1950. I speculate that human activity encour- 
aged the spread of C. nemoralis populations, and this species competitively exterminated C. 
hortensis populations from the intravillan habitats. The frequency of shell colour and banding 
morphs in local populations was similar to those in oceanic Western Europe (56.2 + 18.6% of 
pink shell colour), and may be affected by climatic selection and random drift. There exist small 
areas marked by a high frequency of 00000, 00300, 00345 and 12345 shell banding morphs. 
Their edges were mostly not concordant with areas of geographic distribution. 



INTRODUCTION 

Cepaea nemoralis (L.) is a West-European 
species distributed from southern Scandina- 
via, Lithuania and the Ukraine in the east, to 
Hungary and the northern Balkan Peninsula in 
the south (Schilder & Schilder, 1953, 1957). 
However, it is absent in the highlands of cen- 
tral Europe, in the territories of the Czech Re- 
public and Slovakia. Only Bohemia (the west- 
ern half of the Czech Republic) is crossed by 
the edge of the area of species' continuous 
distribution (Fig. 1). From this region Lozek 
(1956) listed a number of localities scattered 
mostly north of the Labe (Elbe) River where 
С nemoralis was found chiefly at intravillan 
sites. However, the precise borderline of 
the species distribution is impossible to trace 
from the published data. The shell colour 
and banding polymorphism in Bohemian pop- 
ulations has never been quantitatively inves- 
tigated despite the fact that variation in 
marginal populations is of considerable the- 
oretical interest. 

Another common west European species 
is Cepaea hortensis (Müller). It lives in low- 
land and submontane areas of the whole ter- 
ritory of the Czech Republic, at both intravil- 
lan sites and in the open landscape (Lozek, 



1956). There exist indications (see Discus- 
sion) that each Cepaea species may exclude 
the other from occupying the same site. A 
precise delineation of the geographic distri- 
bution of intravillan populations of С horten- 
sis and С nemoralis may contribute to test- 
ing this assumption. A precise study of С 
hortensis distribution in Bohemia is also not 
available. 

The aim of this study was: (1) mapping the 
edge of the С nemoralis distribution, (2) re- 
cording shell colour and banding polymor- 
phism in local populations, and (3) investigat- 
ing the possible interaction of С nemoralis 
with С hortensis populations. Distribution 
and polymorphism in C. nemoralis have been 
the subject of numerous studies (Jones et al., 
1977; Lamotte, 1988). The present work is 
justified by the fact that the occurrence and 
variation were never investigated in the very 
eastern edge of the C. nemoralis area of dis- 
tribution. 



MATERIAL AND METHODS 

The populations of С nemoralis and C. 
hortensis were sampled systematically at in- 
travillan and open landscape habitats of 



111 



112 



HONEK 




О 



GEOGRAPHIC DISTRIBUTION AND SHELL COLOUR 



113 



northern Bohemia in 1989-1991. Towns and 
villages where Cepaea was found are shown 
in Figure 1 . At some localities, the snails were 
sampled at several sites at least 100 m apart. 
The shell colour was classified as pink or 
yellow, although both colours varied largely 
in saturation and hue. In some populations, a 
large proportion of shells was very pale. In 
this case, I lumped all specimens that had 
even a slight trace of pink colour (usually at 
the top of the shell). These were classified as 
"pink," the rest of the animals was classified 
as "yellow." For recording the shell banding 
polymorphism, I used the commonly ac- 
cepted notation. Visible bands are indicated 
from the dorsal side by numbers 1-5, missing 
bands as 0, and fusions between bands are 
indicated by brackets ( ). The sample size 
varied between 6 and 258. Proportions of col- 
our and shell banding forms were calculated 



for populations where at least 15 snails were 
collected. The rare hyalozonate individuals 
(with pale blanks instead of black bands), and 
animals with bands having diluted margins 
(common at some localities) were classified 
as the respective band morphs. Evaluating 
the geographic variation, I compared the pro- 
portions of 00000, 00300, 00345, and 12345 
morphs, regardless of confluences between 
bands. According to the frequency of a 
morph the localities were ranked into four 
categories: (1) zero frequency of the morph, 
(2) low frequency — quartile 1 of the series of 
localities where the morph was present ar- 
ranged in ascending order of the morph per- 
centage, (3) medium frequency — quartile 2 of 
the above series, (4) high frequency — quar- 
tiles 3 and 4 of the above series. 

Details of the frequencies of colour and 
shell banding morphs at different localities 



FIG. 1. The localities of С nemoralis (solid circles), C. hortensis (open circles), and of mixed populations of 
both species (divided circles). The areas of "continuous" distribution of C. nemoralis are delimited by heavy 
lines: above — Libérée LB, left — Litomèt'ice LT, right — Novy Bydzov NB. The area of "scattered" distribution 
is fenced by a dotted line. Insert: Area shown in Fig. 1 projected onto the map of the Czech Republic. The 
edge of the C. nemoralis distribution is shown by a solid line (inside the Czech Republic) and a dashed line 
(after Schilder & Schilder, 1953, 1957). 

Localities of С nemoralis (small figures): 1 Libochovany, 2 Zaihostice, 3 Litomèi'ice, 4 Tfeboutice, 5 
Libèsice, 6 Mlékojedy, 7 Zeletice, 8 Pocaply, 9 Terezin, 10 Nové Kopisty, 11 Bohusovice, 12 Keblice, 13 
Doksany, 14 Lobendava, 15 Lipová, 16 Sluknov, 17 Mikulásovicky, 18 Mikulásovice, 19 Brtníky, 20 Rum- 
burk, 21 Krasná Lipa, 22 Studánka, 23 Dolní Podluzí, 24 Jifetín pod Jedlovou, 25 Rybnisté, 26 Chribská, 27 
Jetfichovice, 28 Kamenicky Senov, 29 Volfartice, 30 Novy Bor, 31 Chotovice, 32 Janov, 33 Sloup, 34 
Castolovice, 35 Manusice, 36 Písecná, 37 Ceská Lipa, 38 Staré Spiavy, 39 Doksy, 40 Mai'enice, 41 
Mai'enicky, 42 Jablonné v Podjestedí, 43 Mimoñ, 44 Stráz pod Raiskem, 45 Hamr, 46 Bi'evnistè, 47 Osecná, 
48 Ki'izany, 49 Ves, 50 Andèlka, 51 Visñová, 52 Minkovice, 53 Víska, 54 Kunratice, 55 Srbská, 56 Jindi'i- 
chovice pod Smrkem, 57 Nové Mésto pod Smrkem, 58 Dolní Rasnice, 59 Krásny Les, 60 Arnoltice, 61 
Frydlant V Cechách, 62 Raspenava, 63 Hejnice, 64 Bíly Potok, 65 Chrastava, 66 Libérée, 67 Vratislavice, 68 
Janov nad Nisou, 69 JosefiJv DijI, 70 Lucany, 71 Tanvald, 72 Velké Hamry, 73 Drzkov, 74 Zásada, 75 
Vrkoslavice, 76 Dalesice, 77 Pulecny, 78 Rychnov u Jablonce nad Nisou, 79 Radio, 80 Hodkovice nad 
Moheikou, 81 Cesky Dub, 82 Milíceves, 83 Slatina, 84 Vrbice, 85 Hradist'ko, 86 Vysoké Veselí, 87 Cho- 
mutice, 88 Ostroméf, 89 Hoi^ice v Podkrkonosí, 90 Lístkovice, 91 Knézice, 92 Zlunice, 93 SekePice, 94 
Smidary, 95 Smidarská Lhota, 96 Janovice, 97 Hlusice, 98 Stary Bydzov, 99 Novy Bydzov, 100 Vysocany, 
1 01 Prasek, 1 02 Mystéves, 1 03 Petrovice, 1 04 Sucha, 1 05 Staré Nechanice, 1 06 Nechanice, 1 07 Boharyné, 
108 Skochovice, 109 Luzec, 110 Nepolisy, 111 MIékosrby, 112 Chiumec nad Cidlinou, 113 Mnichovo 
Hradistè, 114 Sedlist'ka, 115Turnov, 116Zelezny Brod, 117 Bozkov, 118 Sobotka, 119 Nova Рака, 120 
Vrchiabí, 121 Hostinné, 122 Miletín, 123 Pardubice, 124 Libcany, 125 Hradec Králové, 126 Nedèlistè, 127 
Ceská Skalice, 128 Olivétín, 129 Broumov. 

Localities of С. hortensis (large figures): 1 Dolní Habartice, 2 Benesov nad Ploucnicí, 3 Zandov, 4 
Stvolínky, 5 Kravai'e, 6 Ústék, 7 Zahrádky, 8 Jesti'ebí, 9 Holany, 10 Di'evcice, 11 Chium, 12 Vrchovany, 13 
Duba, 14 Pavlícky, 15 Zaksín, 16 Polepy, 17 Host'ka, 18 Snédovice, 19 Stétí, 20 Bélá pod Bezdézem, 21 
Kláster Hradistè, 22 Kosmonosy, 23 Miada Boleslav, 24 Dobrovice, 25 Dolní Bousov, 26 Libán, 27 Chylice, 
28 Kostelec, 29 Kopidlno, 30 Cesov, 31 Chroustov, 32 Chotusice, 33 Dymokury, 34 Záhornice, 35 Mèstec 
Králové, 36 Lovcice, 37 Svijansky Újezd, 38 Hubálov, 39 Radosovice, 40 Jesenny, 41 Jablonec nad Jizerou, 
42 Rovensko pod Troskami, 43 Lomnice nad Popeikou, 44 Libstát, 45 Jilemnice, 46 Horní Branná, 47 Jicín, 
48 Sárovcova Lhota, 49 Lázné Bélohrad, 50 Borovnice, 51 Dolní Kainá, 52 Lanzov, 53 Dvur Králové, 54 
Hoi'icky, 55 Chvaikovice, 56 Resetova Lhota, 57 Jaromér, 58 Semonice, 59 Cernozice, 60 Smii'ice, 61 
Probluz, 62 Stézery, 63 Roudnice, 64 Kosicky, 65 Dobi'enice, 66 Chyst', 67 Rohoviádova Bélá, 68 Holice, 
69 Cernilov, 70 Jasenná, 71 Opocno, 72 Tynisté nad Orlicí, 73 Vamberk, 74 Praha, 75 Karlstejn. 



114 



HONEK 



with an analysis of linkage disequilibria will be 
published in a separate paper (Honèk, in 
prep.). The data may be also obtained on re- 
quest from the author. 



RESULTS 

The Habitats of Cepaea populations 

In Bohemia, typical habitats of С nemora- 
lis are intravillan areas. Most often the snails 
were found at ancient or working cemeteries, 
particularly along the south- and west-facing 
walls. Typical localities were also the railway 
stations surrounded by exuberant weedy 
vegetation. Other sites often populated by С 
nemoralis included small gardens, weed 
stands bordering the margins of quiet 
streets, and intravillan shrubs on south-fac- 
ing slopes. Many sites were periodically dis- 
turbed by human activities: soil cultivation, 
mowing, herbicide application, transport or 
building activities. Despite an intensive 
search, no C. nemoralis populations were 
found outside the intravillan areas. 

Populations of С hortensis in towns and 
villages (Fig. 1 ) occurred in habitats similar to 
those of С nemoralis. Cepaea hortensis gen- 
erally preferred less disturbed sites, and its 
populations were also frequently found in the 
open landscape (localities not shown in Fig. 
1). The preferred rural habitats were hedge- 
rows and shrubs, south-facing slopes with 
mixtures of dicotyledonous and grassy veg- 
etation, and roadside ditches. 

The distribution of Cepaea populations 

Cepaea nemoralis was found at 129 town 
and village localities of northern Bohemia 
(Fig. 1). Most localities were grouped in three 
areas where the species occupied nearly all 
favourable intravillan sites and was present in 
most towns and villages. These areas I call 
"areas of continuous distribution" (Fig. 1 , de- 
limited by solid lines), and refer to by the 
name of the principal included town. The 
largest area of Libérée (LB, localities no. 14- 
81) extends along the northern Bohemian 
frontier and is probably a southern protrusion 
of the area of continuous C. nemoralis distri- 
bution (Fig. 1, insert). Two smaller "island" 
areas of continuous distribution are the area 
of Litomèfice (LT, localities 1-13), and the 
area of Novy Bydzov (NB, localities 82-1 12). 



The boundaries of the areas of "continu- 
ous" distribution could be traced with the 
precision of a few kilometers, that is, the dis- 
tance that divides the neighbouring villages 
of which one is populated by C. nemoralis, 
the other by С hortensis populations. At the 
edge of distribution of both species, for ex- 
ample between Ceská Lipa (Fig. 1, locality 
37) and Doksy (locality 39) in the LB area, or 
along the entire west-south-east edge of the 
NB area, there exist no prominent geo- 
graphic structures which may cause the sep- 
aration of the species. Other portions of the 
boundary are bordered by areas generally 
unfavourable for Cepaea (e.g., volcanic or 
sandstone hills, or large forests). This is also 
the case along the western and eastern sec- 
tions of the boundary of the LB area, and the 
northern sections of the LT and NB areas. 

The LB and NB areas of "continuous" dis- 
tribution are separated by an area of mosaic 
distribution of intravillan C. nemoralis and C. 
hortensis populations, which I refer to as the 
area of "scattered" C. nemoralis distribution 
(Fig. 1, dashed line). Sixteen villages and 
towns with populations of С nemoralis were 
found on this territory. In some towns, for ex- 
ample Pardubice (123) and Hradec Králové 
(125), a C. nemoralis population was found at 
one site, whereas many sites were occupied 
by C. hortensis. 

In total, I found only 14 sites where popu- 
lations of C. nemoralis and С hortensis lived 
together at one place. Five mixed popula- 
tions were found at the area of "scattered" 
distribution, others at the margins of the LB 
(two populations) and NB (seven populations) 
areas of "continuous" distribution. 



Shell Colour and Banding Polymorphism 

The large variation in the proportions of col- 
our morphs had a very localised character. 
Thus, the extent of variation in the frequency 
of the pink form was only slightly smaller 
among 24 sites within the small town of Lito- 
mèfice (9.7-78.3%) than among 73 popula- 
tions of the entire LB area (1 .2-98.4%). The 
average proportion of the pink form was 56.2 
± 18.3%). The figures for particular areas of 
"continuous" distribution differed slightly. 
The highest frequency of pink was in popu- 
lations from the LB area, followed by the LT 
and NB areas (Fig. 2). This difference was 
correlated with greater average altitude (and 
cooler climate) of the LB area (localities at 



GEOGRAPHIC DISTRIBUTION AND SHELL COLOUR 



115 



230-580 m above sea level) than of the LT 
(160-230 m a.s.l.) and NB (190-240 m 
a. s. I.) areas. However, within the LB area the 
regression of the proportion of pink individu- 
als on altitude was not significant (r = 0.006, 
p »0.1) (Fig. 3). 

The frequency of shell banding 00000, 
00300, 00345 and 12345 morphs in local 
populations (Fig. 2) showed typical area ef- 
fects. The distribution of frequencies of the 
00000 morph was right-skewed and popula- 
tions with a high frequency of > 17% were 
found in the LT and LB areas and also at the 
eastern margin of the area of "scattered" 
species distribution (Fig. 4). The populations 
with high frequency > 46.5%, of the 00300 
morph were aggregated in the LT and NB 
areas and also in the north of LB area (Fig. 5). 
The populations with high frequency of 
> 6.6% of 00345 morph were aggregated in 
the LT area and the north LB and west NB 
areas (Fig. 6). The distribution of the 12345 
morph was complementary to distribution of 
other morphs. Populations with high fre- 
quency of > 80.0% of this morph were ag- 
gregated in the south of the LB area. 

The fraction of fused band phenotypes 
within the 12345 morph varied among popu- 
lations. The frequencies of melanic (123)(45) 
and (12345) morphs varied between 0.0- 
45.2% and 0.0-28.4%, respectively, and 
were not correlated (in LB area) with the alti- 
tude of the locality. 

The 00000 phenotype was associated with 
pink colour, and yellow specimens were very 
rare. By contrast, 00300, 00345, and 12345 
morphs were not associated with any colour 
phenotype. Details of linkage disequilibha 
between colour and shell banding morphs 
will be discussed elsewhere (Honék, in 
prep.). 



DISCUSSION 

Spreading of С nemoralis 

Comparing the distribution of C. nemoralis 
populations from before 1950 (Lozek, 1956) 
with this study revealed that most localities 
reported earlier (localities no. 3, 16, 21, 30, 
37, 48, 66, 99, 115) were within the areas of 
"continuous" distribution. The general pat- 
tern of C. nemoralis distribution apparently 
has not changed within the last 50 years, but 
the species became more abundant since 
Lozek (1956; personal communication) qual- 



ified its abundance in the 1 950's as "rare." At 
present, the species also occupies more lo- 
calities than it did earlier. The difference be- 
tween abundance estimates from before the 
1950's and in this study cannot be explained 
by omissions by earlier authors but probably 
indicates an increase of the area of species 
distribution. The change involves southward 
expansion of the LB area, and radial expan- 
sion of LT and NB areas. On the other hand, 
I did not find С nemoralis at three localities 
where it was established before the 1950's: 
Karlovy Vary (Karlsbad) and Zerotin (both 
outside the area shown in Fig. 1) and Ustèk 
(С. hortensis locality no. 6 in Fig. 1). These 
localities are now populated by C. hortensis. 
This indicates extinction of local C. nemoralis 
populations. The causes of extinction are un- 
clear, because ordinary human activity does 
not endanger their survival. The plasticity of 
the distribution of C. nemoralis at the eastern 
edge of the species' distribution area con- 
trasts with its constancy in Western Europe, 
where some populations have persisted, with 
little variation in morph frequency, since the 
neolithic period (Cain & Cook, 1989). 

The factors of fast spreading of an animal 
with a limited dispersion capacity are of in- 
terest. I suppose that human activity may be 
an important factor in species dispersion. 
This follows from a frequent occurrence of 
marginal populations at two typical habitats: 
railway stations and cemeteries. This distri- 
bution may indicate the accidental passive 
transport by man. Climbing onto and falling 
off the railway coaches may disseminate the 
snails. In fact, some marginal populations of 
С nemoralis (e.g. 113, 116, 119, 125) were 
found at railway stations in towns otherwise 
populated by C. hortensis. The occurrence of 
C. nemoralis in cemeteries could be attrib- 
uted to the popular exchange of potted 
plants. The potted plants are usually distrib- 
uted from large gardens to several surround- 
ing villages. The soil infested with the eggs of 
garden populations of C. nemoralis may be- 
come the vehicle of dissemination. 

Relationship to С hortensis 

In fact, C. nemoralis and C. hortensis rarely 
occurred at the same place. In several towns 
(118, 87, 88, 112, 116, 118, 123, 125, 127), С 
hortensis was found at several sites, but C. 
nemoralis inhabited only one place. These 
towns are at the margins of the areas of 



116 



60 



HONEK 

00345 12345 





о 40 



О 40 80 G 40 80 G 40 

MORPH FREQUENCY 



о 40 80 
'Á 



FIG. 2. The frequency of percentages of shell banding morphs 00000, 00300, 00345, 12345 and pink shell 
coloration in populations of C. nemoralis. A — Pooled sample: В — Litomèfice (LT) area of "continuous" 
distribution; С — Libérée (LB) area of "continuous" distribution; D — Novy Bydzov (NB) area of "continuous" 
distribution; E — area of "scattered" distribution. The boundaries of the areas are shown in Fig. 1. 



GEOGRAPHIC DISTRIBUTION AND SHELL COLOUR 



117 



100 



50 



Od 



OL 



• • • 
• • • • 






.1 



• 



• • • 

• • • 

• • • 

• • • • • 

• • • • • 

•• • 



200 



300 



400 

ALTITUDE 



500 



m 600 



FIG. 3. The regression of the percentage of the pink colour form in populations of Libérée (LB) area on the 
altitude (m) above sea level of the locality. Regression: y = -0.01 5x + 63.3, r^ = 0.006, p » 0.1. 



"continuous" distribution or in the area of 
"scattered" distribution. The reverse situa- 
tion when C. nemoralis occurred all over the 
inside of the town and C. hortensis populated 
a few suburban sites, was established at 
Novy Bydzov (99), in the centre of NB area of 
"continuous" distribution. Both examples 
may show stages of invasion of a new locality 
by С nemoralis. At first, C. nemoralis is es- 
tablished at one place and from there it 
spreads, exterminating C. hortensis popula- 
tions. At a given site, the transition is perhaps 
quick, as mixed populations usually contain a 
majority of one species, either С hortensis 
(28, 83. 85, 86) or С nemoralis (69, 91, 120). 
There exists some experimental evidence 
for competition superiority of C. nemoralis 
over C. hortensis (Cameron & Carter, 1979, 
Tilling, 1985a, b), and competitive exclusion 
has been proposed in explaining the distribu- 
tion of both species (Boycott, 1934; Cain, 
1983). The situation in Bohemia contrasts 
with that in Western Europe, where mixed 
populations may coexist for a long time (Cain 
& Currey, 1963a; Cain, 1983). This difference 
may be due to the fact that in the western 
part of its distribution area С nemoralis lives 
in the extravillan landscape where C. horten- 



sis may resist its competition. Also, in Bohe- 
mia C. hortensis populations live outside the 
towns where intravillan sites are all occupied 
by C. nemoralis. 

The examples of invasion of a locality oc- 
cupied by one Cepaea species by the other 
species are few. Well documented is a recent 
(between 1961 and 1985) substitution of С 
nemoralis by С hortensis on severeal sites at 
Marlborough Downs, England (Cain & Cur- 
rey, 1963b; Cowie & Jones, 1987). The trend 
observed in this non-urban area may be a 
consequence of the change of the microcli- 
mate following the change of the vegetation 
cover. A dense and tall vegetation may favour 
the occurrence of С hortensis, which makes 
better use of solar radiation and is capable of 
exploiting shade places. The microclimate 
might favour also the changes in Bohemian 
populations because intravillan sites where 
C. nemoralis probably replaced C. hortensis 
are generally warmer than the sites in the 
open landscape occupied by C. hortensis. 

Colour and Shell Banding Polymorphism 

The study of C. nemoralis variation is a 
problem that has resisted final solution de- 
spite the large body of accumulated data 



118 



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HONEK 




GEOGRAPHIC DISTRIBUTION AND SHELL COLOUR 



121 



(Schilder & Schilder, 1 953, 1 957; Jones et al., 
1977; Cain, 1983; Lamotte, 1988). Typical 
features of this polymorphism are very local 
differences in the proportion of morphs 
(Wolda, 1969a, b), and the "area effects," 
that is high frequency of a phenotype in a 
limited area (Cain & Currey, 1963b). Area ef- 
fects have been observed for both shell co- 
lour and banding polymorphism (Khemici et 
al., 1989; Lamotte et al., 1989; Ratel et al., 
1989). The factors of differences in morph 
proportions may be random population pro- 
cesses (Lamotte, 1951, 1952) or selection by 
climatic or substrate factors (Currey & Cain, 
1968; Cameron et al., 1977; Khemici et al., 
1989; Mazon et al., 1988, 1989) or visual 
predators (Cain & Sheppard, 1950). 

Random processes have probably influ- 
enced the composition of some of our iso- 
lated populations. Morph frequencies may be 
influenced by genetic drift when populations 
were established from a small number of 
founders. An example may be the population 
at the railway station at Nova Рака (119), 
which consisted of 95.6% of pink 00300 in- 
dividuals. 

Climatic effects contribute to maintaining 
the frequencies of shell colour forms. Popu- 
lations from areas with oceanic climate are 
mostly pink in contradistinction to the mostly 
yellow populations of areas with Mediterra- 
nean climate (Mazon et al., 1988; Vicario et 
al., 1988). Multivariate analysis of climatic 
and substratum data revealed that these fac- 
tors contribute also to maintaining small dif- 
ferences in shell colour frequencies under 
oceanic climate (Khemici et al. 1989, Ratel et 
al. 1989). 

The average proportion of pink individuals 
in Bohemian populations (56.2%) was similar 
to that in oceanic Western Europe (about 
60% of the pink form) and far greater than 
in Mediterranean populations (with only 20- 
30% of pink form, Lamotte, 1988; Mazon et 
al., 1988). Typical for Bohemian populations 
is also the absence of the yellow 00000 phe- 
notype, which is the most adapted one to 
warm conditions. A demonstration of climatic 
effects on diversification of morph propor- 
tions among Bohemian populations would 
require more microclimatic and orographic 
data. An indication of such effects was the 
increased frequency of the pink form in hilly 
LB compared to lowland LT and NB areas. 

No explanation has been found for the area 
effects shown by the 00000, 00300, 00345, 
and 12345 morphs. The role of visual préda- 



tion on maintenance of differences between 
populations is difficult to evaluate. The local- 
ities of С nemoralis in Bohemia become cov- 
ered mostly by sparse vegetation (weeds, 
ornamental plants), which makes a rather 
uniform optical background for avian preda- 
tors. Under such conditions, visual prédation 
is not likely to create important differences in 
morph proportions among local populations 
of Cepaea. Anyway, the results do not con- 
tradict the classical theory of the role of visual 
selection in maintaining Cepaea polymor- 
phism (Cain & Sheppard, 1950, 1954). The 
remains of crushed shells were found at only 
15 collection sites. This paucity of crushed 
shells parallels the results of other studies 
(e.g. Cowie & Jones, 1987) and may caused 
by preference of avian predators for juveniles 
(cf. Wolda, 1972; Wolda & Kreulen, 1973). A 
comparison of morph frequency in adult 
crushed shells and in living animals could be 
made only at one locality (Arnoltice 60). There 
was no significant difference in proportion of 
colour and banding morphs among living an- 
imals and dead shells. 



ACKNOWLEDGEMENTS 

I thank Prof. A.J. Cain, Prof. M. Lamotte 
and Dr. V. Lozek for critical reading of my MS 
and many valuable comments. 



LITERATURE CITED 

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CAIN, A. J., 1983, Ecology and ecogenetics of ter- 
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CAIN, A. J. & L. M. COOK, 1989, Persistence and 
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CAIN, A. J. & J. D. CURREY, 1963a, Area effects in 
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CAIN, A. J. & J. D. CURREY, 1 963b, Area effects in 
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CAIN, A. J, & P. M. SHEPPARD, 1950, Selection in 
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CAIN, A. J. & P. M. SHEPPARD, 1954, Natural se- 
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CAMERON, R. A. D. & M. A. CARTER, 1979, Intra- 
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CAMERON, R. A. D., P. WILLIAMSON & D. \. MOR- 
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COWIE, R. H. & J. S. JONES, 1987, Ecological 
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97. 

CURREY, J. D. & A. J. CAIN, 1968, Studies in 
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JONES, J. S., B. H. LEITH & P. RAWLINGS, 1977. 
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KHEMICI, E., J. GENERMONT & M. LAMOTTE, 
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LAMOTTE, M., 1951, Recherches sur la structure 
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LAMOTTE, M., 1952, Le rôle des fluctuations for- 
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LAMOTTE, M., 1988, Facteurs influençant la diver- 
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LAMOTTE, M., I. KASSEM & J. GENERMONT, 
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LOZEK, V., 1956, KIÍC ceskoslovenskych mékkysiJ. 
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Slovenskej Akademie Vied. Bratislava. 

MAZON, L I., M. A. M. DE PANCORBO, A. VI- 
CARIO, A. I. AGUIRRE, A. ESTOMBA & С M. 
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tions of Cepaea. Génétique Selection et Evolu- 
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MAZON, L. I., A. VICARIO, M. A. M. DE 
PANCORBO, A. I. AGUIRRE, A. ESTOMBA & С 
M. LOSTAO, 1988, North/south differentiation in 
the distribution of Cepaea nemoralis in Spain. 
Heredity, 61: 189-197. 

RATEL, M. O., J. GENERMONT & M. LAMOTTE, 
1989, Relation entre polymorphisme et milieu 
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la region Parisienne. Bulletin de la Société 
Zoologique de France, 1 13: 145-154. 

SCHILDER, F. A. & M. SCHILDER, 1953, Die Bän- 
derschnecken. Eine Studie zur Evolution der 
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SCHILDER, F. A. & M. SCHILDER, 1957, Die Bän- 
derschnecken. Eine Studie zur Evolution der 
Tiere. Schluss: Die Bänderschnecken Europas. 
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70. 

TILLING, S. M., 1985b, The effect of interspecific 
interaction on spatial distribution patterns in ex- 
perimental populations of Cepaea nemoralis (L.) 
and C. hortensis (Mull.). Biological Journal of the 
Linnean Society, 24: 71-81. 

VICARIO, A., L \. MAZON, A. AGUIRRE, A. ES- 
TOMBA & С LOSTAO, 1988, Vanation in popu- 
lations of Cepaea nemoralis (L.) in North Spain. 
Biological Journal of the Linnean Society, 35: 
217-227. 

WOLDA, H., 1969a, Fine distribution of morph fre- 
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Groningen. Journal of Animal Ecology, 38: 305- 
327. 

WOLDA, H., 1969b, Stability of a steep dine in 
morph frequencies of the snail Cepaea nemoralis 
(L.). Journal of Animal Ecology, 38: 623-635. 

WOLDA, H., 1972, Ecology of come experimental 
populations of the landsnail Cepaea nemoralis 
(L.). I. Adult numbers and adult mortality. Neth- 
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WOLDA, H. & D. A. KREULEN, 1973, Ecology of 
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ology, 23: 168-188. 

Revised Ms. accepted 18 October 1994 



MALACOLOGIA, 1995, 37(1): 123-132 

KARYOTYPE ANALYSIS AND GENOME SIZE IN THREE MEDITERRANEAN 
SPECIES OF PERIWINKLES (PROSOBRANCHIA: MESOGASTROPODA) 

R. Vitturi\ A. Libertini^, M. Panozzo^ & G. Mezzapelle^ 

ABSTRACT 

The diploid chromosome number 2n = 34 has been determined in early developing embryos 
of L. saxatilis and male gonads of L. (Melaraphe) punctata both from the Mediterranean Sea. 
The diploid value 2n = 33 occurred in spermatocytes of L (Melaraphe) neritoides specimens 
from the Lagoon of Venice. As previously reported for L. neritoides from the Sicilian coast, a 
male XO sex-determining mechanism seems to operate also in the population of the same 
species here studied. Variation in the number of NOR-bearing chromosomes per cell has been 
detected in both L. saxatilis and L (Melaraphe) neritoides. Flow cytometric DNA analysis indi- 
cates that L. saxatilis and L. (Melaraphe) neritoides are endowed by almost equal genome sizes, 
whereas L. (Melaraphe) punctata exhibits about 60% of their values. 

Key words: periwinkles, karyology, genome size, Mediterranean Sea. 



INTRODUCTION 

Periwinkles are mesogastropod molluscs 
belonging to the genus LIttohna which inhabit 
rocky coasts and lagoon brackish waters. In 
the Mediterranean, this genus is represented 
by three species: L. saxatilis (Olivi, 1792), L. 
neritoides (Linnaeus, 1758) and L punctata 
(Gmelin, 1791). On the basis of their repro- 
duction, embryogenesis, and morphology of 
the radula and penis, the former belongs to 
the subgenus Littohna, whereas the others 
are grouped in the subgenus Melaraphe 
(Nordsieck, 1968; Torelli, 1982). 

Cytogenetically, two Mediterranean popu- 
lations of L. neritoides (Thiriot-Quievreux & 
Ayraud, 1982; Vitturi et al., 1988) and three 
North Sea populations of L. saxatilis, from 
western Sweden, northern England (Janson, 
1983) and the Barentz Sea (Birstein & Mikhai- 
lova, 1990), have been investigated. Never- 
theless, the results of these studies do not 
agree. More precisely, the diploid number of 
34 chromosomes was proposed by Thiriot- 
Quievreux & Ayraud (1982) for L. neritoides 
males from Villefranche-sur-Mer, Provence, 
France, whereas 2n = 33 was found in male 
specimens from Palermo, Sicily, Italy (Vitturi 
et al., 1988). In the latter population, the oc- 
currence of an unpaired chromosome in 
spermatocytes, along with n = 17 bivalents in 
the female, made the authors hypothesise a 
male XO sex-determining mechanism oper- 
ating in this species. 



Moreover, although Janson (1983) and 
Birstein & Mikhailova (1990) agree upon the 
chromosome number (34 in the diploid set) of 
three different populations of L. saxatilis, 
there are small differences related to the 
karyotype morphology. In fact, three small 
chromosome pairs were seen as subtelocen- 
tric in the Swedish population (Janson, 1983), 
whereas the same pairs were found to be 
most likely telocentric in the strain from the 
Barentz Sea (Birstein & Mikhailova, 1990). 

Karyological investigation in the present 
report includes: (1) analysis of L. neritoides 
male specimens from the Lagoon of Venice, 
northeastern Italy, in order to verify if the 
male XO sex-mechanism also occurs in this 
geographical location; (2) a comparison 
among the karyotypes of L. saxatilis from the 
Mediterranean Sea and from the North Sea 
previously described (Janson, 1983; Birstein 
& Mikhailova, 1990); and (3) a preliminary cy- 
togenetic characterisation of L. punctata, 
which is still unknown. 

Moreover, in order to better understand 
karyological relationships in Littorinidae, nu- 
cleolar organizer regions (NORs) of L. saxati- 
lis and L. neritoides as well as genome sizes 
in the three species have been investigated. 

MATERIALS AND METHODS 

Several specimens of the brooding L. sax- 
atilis and sexually mature L. (Melaraphe) neri- 
toides were collected along the dock base- 



'' Institute of Zoology, University of Palermo, Via Archirafi 18-90123, Palermo, Italy. 

^CNR-lnstitute of Marine Biology, Riva 7 Martiri 1364/A, Venice, Italy. 

^National Institute of Cancer Research, Biotechnological Section, Via Gattamelata 64, Padua, Italy. 



123 



124 VITTURIETAL 

TABLE 1. Counts of mitotic spreads in three Mediterranean periwinkles species. 



SPECIES 



ORIGIN 



2n = 21 22 23 24 25 26 27 28 29 30 31 32 33 34 TOTAL 



1 



Littohna saxatilis Lagoon of Venice 
Littorina (Melaraphe) 

punctata Gulf of Palermo — — — — 

Littorina (Melaraphe) 

neritoides Lagoon of Venice — — — — 



1 2 27 32 

2 1 20 24 

2 — 1 18 — 21 



merits, in Venice, Italy, on October 1991 and 
April 1992, respectively. Sexually mature 
specimens of L. (Melaraphe) punctata were 
sampled from July 1991 to August 1993 on 
rocky shores at Sferracavallo, Palermo Dis- 
trict, Italy. Identifications were made accord- 
ing to the guidelines of Parenzan (1970) and 
Torelli (1982), and voucher shells of five indi- 
viduals per species were deposited at the 
Museum of the Institute of Zoology, Univer- 
sity of Palermo. 

Mitotic metaphase chromosomes of L. 
saxatilis were obtained from early developing 
embryos extracted from 20 different females 
and treated with 0.025% colchicine in 0.075 
M KCl solution for 20 min according to the 
air-drying technique. The same procedure 
was applied to the testes of 1 5 specimens of 
L. (Melaraphe) neritoides and 30 of L. (Mela- 
raphe) punctata to obtain diakinetic bivalents 
and spermatogonial metaphases. Slides 
were stained in 5% Giemsa-phosphate 
buffer solution (pH 6.8), observed, then de- 
stained in ethanol and restained with silver 
nitrate according to the colloidal 1-step 
method (Howell & Black, 1980). 

In order to obtain the karyogram of L. sax- 
atilis and L. (Melaraphe) neritoides, the chro- 
mosomes of five plates per species were cut 
and paired on the basis of decreasing size 
and centromere position. Chromosomes 
were measured and classified by arm-ratio 
(longer/short arm) following the nomencla- 
ture proposed by Levan et al. (1964). 

Genome size was evaluated through flow 
cytometric assay. From dissected mantle of 
8-20 specimens per species, a cell suspen- 
sion was obtained by a 5 min hypotonic treat- 
ment with 0.075 M KCl solution. Cells were 
filtered through a 30-цт mesh, then fixed in 
70% ethanol and centrifuged twice at 800 g 
adding new fixative every time. Samples 
were stored at -20°C. 

A day before cytofluorimetric analysis, 
cells were centrifuged again and resus- 
pended into 1 ml of solution containing 
0.12% sodium citrate, 0.005%) propidium io- 



dide and 0.1% RNase. RNA digestion was 
performed at 37''C for 30 min, while staining 
lasted overnight at 4°C. Gill cells of the blue 
mussel {Mytilus edulis) were prepared in the 
same manner and used as standard. Control 
assigned DNA content was 3.2 pg according 
to Hinegardner (1974). An EPICS-C flow cy- 
tometer (Coulter Electronics, Hialeah, Flor- 
ida) was employed for DNA content mea- 
surements. 

A 488-nm argon ion laser was used for ex- 
citation and total red fluorescence emission 
was measured. At least three samples per 
species each containing more than two thou- 
sand cells were employed. Conditions of 
analysis were set in order to obtain the modal 
value of blue mussel at the channel 50 in a 
256-channel DNA histogram. 

The samples of periwinkle species were 
run both with and without control cells; be- 
cause data distribution of reference and test- 
ing nuclei were partially overlapped, only in- 
dividual histograms are shown. 



RESULTS 

The diploid value 2n = 34 has been found 
in both L. saxatilis and L. (Melaraphe) punc- 
tata from counts of 32 and 24 metaphases 
respectively (Table 1). A few aneuploid 
spreads displaying a chromosome number 
lower than the mode were also encountered. 
These might be related to technical short- 
comings. 

Littorina saxatilis complement (Figs. 1, 2; 
Table 2) consisted of all bi-armed pairs 
(M+SM) except for pairs 4 and 6, which were 
mono-armed (ST). However, pairs 3, 7, and 
12 were characterized by arm ratio on the 
border line between SM and ST and thus, 
considering their confidence limits (respec- 
tively 1.53-2.01, 1.34-2.20 and 2.47-3.29), 
these chromosome pairs may not be attrib- 
uted to one or the other chromosome class. 

NOR location and variation in number of 
NOR-bearing chromosomes per cell were 



KARYOTYPES OF PERIWINKLES 



125 



íllttttu 



' 2 3 

Il le iE «i 14 H Kl 



12 13 



M fi n ii iâ li и 



t it *« 



3 . a Ь 



a b 






FIG. 1. Karyogram obtained from five mitotic metaphases of L. saxatilis. 

FIG. 2. Giemsa stained representative karyotype of L. saxatilis. 

FIG. 3. Different NOR phenotypes (A, B, C, D) of L. saxatilis. 

FIG. 4. Giemsa stained spermatocyte bivalents at diakinesis of L. (Melaraphe) punctata. 



detected in L. saxatilis by silver staining. chromosomes belonging to pairs 4 ("a" 
NORs were located on the short arms in three type), 6 ("b" type) and 15 ("c" type). In the 
different types of silver positively stained first case, NOR was in a large-sized subtelo- 



126 



VITTURI ET AL. 



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KARYOTYPES OF PERIWINKLES 



127 



centric chromosome and seemed to be ter- 
minally or sub-terminally located in con- 
densed (Fig. ЗА) and decondensed (Fig. 3B) 
chromosomes. In the second case it was ter- 
minal in a medium-large subtelocentric chro- 
mosome, and finally it resulted to be terminal 
in a small-sized submetacentric chromo- 
some. Four NOR phenotypes, differing for 
the number of chromosomes involved in nu- 
cleolus organization, were found: one char- 
acterized by four chromosomes (a, a, b, с in 
two spreads) (Fig. ЗА), two by three chromo- 
somes (a, a, b and a, b, c, in 7 and 5 plates, 
respectively) (Fig. 3B, C) and one by two (a, b 
in six spreads) (Fig. 3D). 

In L. punctata, notwithstanding several at- 
tempts during three reproductive seasons 
(1991-1993), no slides gave spermatogonial 
metaphases useful to define the karyotype 
morphology of this species due to the over- 
condensation of mitotic chromosomes. 
Overall, the diploid number tendel tube 2n = 
34 (Table 1). The haploid number was n = 17 
(Fig. 4), and no heteropycnotic elements 
were identified. 

Counts of 21 spermatogonial metaphases 
resulted in the diploid number 2n = 33 in L 
(Melaraphe) neritoides from the Lagoon of 
Venice (Fig. 5). The karyogram (Fig. 6, Table 
2) consisted of 16 autosomal pairs, 12 of 
which were bi-armed and four mono-armed 
(pairs 4, 5, 6, 8), and one small unpaired sub- 
metacentric element about 1 ¡am long. 

After silver staining, spermatogonial meta- 
phases showed the occurrence of either three 
or two NOR-bearing chromosomes per plate 
referred as to two distinct NOR phenotypes. 
The former consisted of two small-sized me- 
tacentric chromosomes (pair 1 6) with terminal 
NORs and a large subtelocentric (pair 6) with 
telomeric NORs on the short arms designated 
"a," "a" and "b," respectively (Fig. 7A), and 
was observed in 15 spreads. The latter in- 
cluded two small-sized metacentric NOR- 
bearing chromosomes always similar to those 
previously identified as "a" (Fig. 7B), and this 
was found in 12 spreads. 

Analysis of diakinetic plates showed 16 
bivalents plus one small-sized submetacen- 
tric. The latter being characterized by the 
same morphology of the unpaired element 
observed in mitotic metaphases, was inter- 
preted as "univalent" (Fig. 8, arrow). 

A typical fluorescence distribution histo- 
gram in cell samples of the three periwinkle 
species and the control are given in Fig. 9 
(A-D). Each littorinid species is characterized 



by two peaks. The first one represents diploid 
cells while the second one — localized at a 
double distance from the axes origin (tetra- 
ploid peak) — is probably due to cell aggrega- 
tion rather than G2-M phase cells. The refer- 
ence exhibits one peak only. 

Red fluorescence emission measurements 
are summarized on Table 3. They indicate 
that L. saxatilis and L. (Melaraphe) neritoides 
are endowed by almost equal genome sizes 
(estimated haploid DNA content of 1 .352 and 
1.376 picograms, respectively), whereas L. 
(Melaraplie) punctata exhibits about 60% of 
these values (0.811 pgs). 



DISCUSSION 

Karyological data concerning all periwin- 
kles of the genus Littorina studied to date are 
briefly summarized on Table 4. Interestingly, 
a diploid number 2n = 33 occurs in males of 
Littorina (IVIelaraplie) neritoides from the La- 
goon of Venice. This result, and a karyotype 
very similar to that observed for L. (Melara- 
phe) neritoides from the Sicilian coast (Vitturi 
et a!., 1988), supports a male XO sex chro- 
mosome system presumably operating in 
this species. Moreover, as previously argued 
(Vitturi et al., 1988), this result does not agree 
with 2n = 34 suggested by Thiriot-Quievreux 
& Ayraud (1 982) for the males of L. (Melara- 
phe) neritoides from Villefranche-sur-Mer, 
France. Because of the hypothesis of a chro- 
mosomal polymorphism in this species has 
already been excluded (Vitturi et al., 1988), a 
karyotype revision of the French population 
would be desirable. 

Male XO sex determination mechanism 
has been described in some grasshoppers 
(Cabrero et al., 1985; Vitturi et al., 1993) and 
fishes (Chen, 1969; Le Grande, 1975). How- 
ever, according to our knowledge, it has 
never been reported in mesogastropods, be- 
cause neritid species, possessing this sex- 
determination mechanism (Vitturi & Catalane, 
1988, and authors quoted by them) belong 
to Archaeogastropoda (Franc, 1968; Boss, 
1982). 

The same chromosome number (2n = 34) 
but with small differences in karyotypes have 
been found in three out of four L. saxatilis 
populations analyzed so far. Observed differ- 
ences are to be probably related to the fact 
that some chromosome pairs may be close 
to the limits between different chromosome 
categories. 



128 



VITTURI ET AL 



te It II Ù Кй «I 

Il M H t$ tu II 

13 '* 15 ,6 ,7 

#« Xt li tl « 



■■ f 1 1 1 1 i I H t m t 



8 






/.i 






FIG. 5. Giemsa stained karyotype from male gonads of L. (Melaraphe) neritoides. 

FIG. 6. Karyogram obtained from five spermatogonia! metaphases of L. (Melaraphe) neritoides. 

FIG. 7. NOR ptnenotypes (A and B) of L. (Melaraphe) neritoides (g = giemsa stained and n = silver stained). 

FIG. 8. Diakinetic bivalents from male gonads of L. (Melaraphe) neritoides (arrow indicates the unpaired 

chromosome). Scale for figures from 1 to 8: 10 (am = 26 mm 



Considering NOR patterns determined for 
L. (Melaraphe) neritoides and L. saxatilis, 
some considerations can be drawn: 

1. intra-specific polymorphism due to dif- 
ferent number of silver-positive chro- 
mosomes per cell occurs in both spe- 
cies; 

2. chromosomal location of active NOR 
sites differs from one species to an- 
other; 



3. at least three chromosome pairs are in- 
volved in nucleolus organization in L. 
saxatilis, whereas only two operate in L. 
(Melaraphe) neritoides. This implies a 
smaller variation of NOR patterns in the 
second species. 

On the whole, data from the literature doc- 
ument a wide distribution of NOR polymor- 
phism within animal kingdom (Foresti et al., 
1981; Gold & Amemiya, 1986; King et al., 



KARYOTYPES OF PERIWINKLES 



129 




red fluorescence 




Littorina (Uelaraphe) punctata 



Liltorina saxátil is 




Littorina (Uelaraphe) neriloides 



Uytilus edulis 



FIG. 9. A-D. Histograms of red fluorescence emission in cell suspensions obtained from three species of 
Littorinidae and Mytilus edulis (control). A: L. (Melaraphe) punctata; B: L. saxatilis; C: L. (Melaraphe) neri- 
toides; D: Mytilus edulis. Red fluorescence emission and number of scored cells are expressed in arbitrary 
units. 



1990; Vitturi et al., 1991a). Particularly, in 
mollusks, intraspecific NOR variations have 
been described for two prosobranch gastro- 
pods (Vitturi & Catalane, 1989, 1990), two 
pulmonates (Vitturi et al., 1 991 b; Vitturi, 1 992) 
and four oysters (Thihot-Ouievreux & Insua, 
1992; Insua & Thihot-Quievreux, 1993). 

Haploid genome sizes (C-value) vary from 
0.8 to 1.3 pg in five littorinid species (Hine- 
gardner, 1974; present paper), whereas the 
diploid chromosome number is 34, except 
for males of L. (Melaraphe) neritoides. Ob- 
tained results allow us to speculate that large 
differences in genome size of periwinkles and 



loss or accumulation of DNA occur within 
chromosomes without changing their num- 
ber. As already reported for other organisms 
(Hutchinson et al., 1 980; Gold & Prince, 1 985; 
Olmo et al., 1989; Vitturi et al., 1993), ob- 
served C-value variability ought to reflect pri- 
marily gain or losses of repeated DNA se- 
quences. 

As in littorinid species, wide genome size 
variations with no substantial change in chro- 
mosome number have been already reported 
among species of the same genus in culicid 
mosquitoes (Díptera) (Nagesh Rao & Ral, 
1990) and leaf beetles (Coleóptera, Chry- 



130 



VITTURI ET AL. 



TABLE 3. Genome size evaluation in three periwinkle species. Relative fluorescence is referred to 
Mytilus edulis 







Fluorescence in 












Arbitrary 


Units 


Percentage 


Estimate 






Number of 


Average 


Standard 


of Relative 


Haploid DNA 


Standard 


Species 


Samples 


modal Value 


Deviation 


Fluorescence 


Content (pgs) 


Deviation 


Littohna (Melaraphe) 














punctata 


3 


25.333 


0.471 


50.667 


0.811 


0.0301 


Littohna (Melaraphe) 














nehtoides 


3 


43 


0.816 


86 


1.376 


0.0522 


Littohna saxatilis 


4 


42.250 


0.829 


84.500 


1.352 


0.0531 



TABLE 4. Chromosome numbers in six species of the genus Littohna 



Species 


n 


2n 


Origin 


Reference 


L. brevicula 


17 


— 


Japan 


Nishikawa, 1962 


L. sthgta 


17 


34 


Japan 


Nishikawa, 1962 


L. nehtoides 


17 


34 


Provence, France 


Thiriot-Quievreux & Ayraud, 1982 


L. nehtoides 


17 


33 


Lagoon of Venice, Italy 


Present paper 


L. nehtoides 


17 


33 


Gulf of Palermo, Italy 


Vitturi et al., 1988 


L. punctata 


17 


34 


Gulf of Palermo, Italy 


Present paper 


L. saxatilis 


17 


34 


Cornwall, England 


Jansen, 1983 


L. saxatilis 


17 


34 


Northern Sea, Sweden 


Janson, 1983 


L. saxatilis 


17 


34 


Barents Sea 


Birstein & Mikhailova, 1990 


L. saxatilis 


— 


34 


Lagoon of Venice, Italy 


Present paper 


L. obtusata 


— 


34 


Northern Sea, Sweden 


Janson, 1983 



somelidae) (Petitpierre & a!., 1993). Further- 
more, no direct correlation between DNA 
content and chromosome number were ar- 
gued also for pleurocerid snail genus Semi- 
sulcospira (Mesogastropoda) (Nakamura & 
Ojima, 1990). 

Although karyological data for L. punctata 
are limited to the diploid chromosome num- 
ber (2n = 34) and spermatocyte bivalent mor- 
phology, they allow us to exclude a XO sex- 
determining mechanism for this species. 
Hence, the wide karyological differences (ge- 
nome size and presence of sex chromo- 
somes) between L. punctata and L. neh- 
toides make location of these species in the 
same subgenus (Nordsieck, 1968; Torelli, 
1982) unjustified. Alternatively, in accordance 
with Rosewater (1970), the taxon Melaraphe 
should contain only L. nehtoides, which dif- 
fers from all other littorinids by a pair of cusps 
on the basal part of the central tooth in the 
radula. 

The three species of Littohna here studied 
display a great variability when different cy- 
togenetical parameters (i.e., karyotype mor- 
phology, NOR patterns, sex chromosomes, 
genome size) are considered, and, therefore. 



karyology may be very useful in order to de- 
fine the frequently rearranged taxonomy of 
the genus (Bändel, 1974). 



ACKNOWLEDGEMENTS 

Financial support by the ministère per Г 
Université e la Ricerca Scientifica e Tecno- 
lógica (60%, 1992-93), Roma, is gratefully 
acknowledged. 



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MALACOLOGIA, 1995, 37(1): 133-156 

POPULMION GENETICS AND SYSTEMATIC STATUS OF ONCOMELANIA 
HUPENSIS (GASTROPODA: POMATIOPSIDAE) THROUGHOUT CHINA 

George M. Davis\ Zhang Yi^, Guo Yuan Hua^, & Christina Spolsky'' 

ABSTRACT 

The coevolved relationships of populations considered to be Oncomelania hupensis through- 
out China with Schistosoma japonicum are of interest to evolutionary biologists and consider- 
able importance to medical science relative to understanding the differentiation of the parasite 
throughout its range. As populations of Oncomelania dispersed and diversified in a direction 
from Burma-western Yunnan, China, throughout China to Japan and the Philippines, the par- 
asite has had to modify genetically with the genetically changing snail populations or become 
regionally extinct. This hypothesis predicts that measures of genetic distance among snail 
populations parallel genetic diversification among parasite populations. Our question here is: to 
what extent have populations of Oncomelania diverged genetically throughout China, and what 
are the implications for systematic status of the populations? 

Measures of population divergence for Oncomelania can be derived from shell characters, 
anatomical characters, or molecular genetic distances. In this paper, we explore genetic di- 
vergence based on allozyme data involving 14 populations that are widespread throughout 
China, are in divergent drainage systems, and have different shell phenotypes. We find con- 
siderable genetic differentiation occurring throughout China. We also find coherent discernable 
patterns to the genetic differentiation. Careful examination of these patterns provides evidence 
for one case of cross-country transport of snails, and for the existence of three exceptional 
populations in which hybridizations between subspecies may have occurred. Excluding these 
four populations, patterns of genetic differentiation are in general correlated with geographic 
distribution and shell sculptural and shape characters. These patterns thus serve as the basis 
for subdivision of O. hupensis into three discrete subspecies. O. h. robertsoni, O. h. tangi, and 
O. h. hupensis. 



INTRODUCTION 

The rissoacean gastropod genus Oncomel- 
ania is restricted to Asia and has two species 
based on morphological criteria (reviewed in 
Davis, 1994); Oncomelania hupensis poly- 
typic species distributed from northern Burma 
(fossil), western China to Japan, Philippines, 
and Sulawesi, and O. minima in northwestern 
Honshu, Japan. The genus is one of eight 
genera of the Pomatiopsidae: Pomatiopsinae 
deriving from a Gondwanian origin (Davis, 
1979). The other genera are now found in 
South Africa, South America, Australia, Ja- 
pan, and the U.S.A. The genus in the U.S.A., 
Pomatiopsis, derived from Oncomelania of 
Japan. 

Oncomelania is of considerable interest to 
very different groups of people. To the spe- 
cialist in tropical medicine and parasitology, 
O. hupensis is associated with the transmis- 
sion of the human blood worm Schistosoma 



japonicum. The two species of Oncomelania 
also transmit different species of the lung 
fluke Paragonimus (Davis et al., 1994). For 
the systematist, variation in size and shell 
sculpture throughout the range of the genus 
has been the basis for debates about the 
number of genera and species involved 
(Bartsch, 1936a; Abbott, 1948; Davis, 1971; 
Kang, 1981, 1985; Liu et al. 1981; Lou et al. 
1982). The genus now plays a central role in 
the debate of defining what a species is. 
Does one today recognize polytypic species 
or subspecies; to what extent should one rely 
on measures of genetic distance to define 
species (Woodruff et al., 1988; Davis, 1994)? 
The coevolved relationships of populations 
considered to be Oncomelania hupensis 
throughout China with Schistosoma japoni- 
cum are of interest to evolutionary biologists 
and considerable importance to medical sci- 
ence relative to understanding the differenti- 
ation of the parasite throughout its range (re- 



^ Academy of Natural Sciences of Philadelphia, 1900 Benjamin Franklin Parkway, Philadelphia PA 19103. 
^institute of Parasitic Diseases, Chinese Academy of Preventive Medicine, Shanghai, China. 



133 



134 



DAVIS, ZHANG, GUO & SPOLSKY 



viewed by Davis, 1992). As populations of 
Oncomelanla dispersed and diversified in a 
direction from Burma-western Yunnan, 
China, throughout China to Japan and the 
Philippines (Davis 1979), the parasite has had 
to modify genetically with the genetically 
changing snail populations or become re- 
gionally extinct. This hypothesis predicts that 
measures of genetic distance among snail 
populations parallel genetic diversification 
among parasite populations. 

Measures of population divergence for On- 
comelania can be derived from shell charac- 
ters, anatomical characters, or molecular ge- 
netic distances. In this paper, we explore 
genetic divergence based on allozyme data 
involving 14 populations that are widespread 
throughout China, are in divergent drainage 
systems, and have different shell pheno- 
types. We find considerable genetic differen- 
tiation occurring throughout China. We also 
find coherent discernable patterns to the ge- 
netic differentiation. Careful examination of 
these patterns provides evidence for one 
case of cross-country transport of snails, and 
for the existence of three exceptional popu- 
lations in which hybridizations between sub- 
species may have occurred. Excluding these 
four populations, patterns of genetic differ- 
entiation are in general correlated with geo- 
graphic distribution and shell sculptural and 
shape characters. These patterns thus serve 
as the basis for subdivision of O. hupensis 
into three discrete subspecies: O. h. robert- 
soni, O. h. tangí, and O. h. hupensis. 

MATERIALS AND METHODS 
Specimens Studied 

Two groups of populations were studied 
seven months apart: all snails were alive 
when brought to the United States by Dr. 
Quo. They were collected by members of lo- 
cal anti-epidemic stations throughout China 
and sent to Dr. Quo in Shanghai. The 14 lo- 
calities sampled are listed in Table 1 and are 
shown in Figure 1 . Group I represents seven 
populations from the most geographically 
separated locations in China collected in No- 
vember 1984. Group II snails, collected in 
November 1985 were from central to eastern 
China, with populations concentrated in the 
Hubei-Hunan-Anhui triangle. 

Shell categories are based on the major 
phenotypic classes of variants (Figs. 2-5): (1) 
smooth and no varix = S; (2) smooth but with 



pronounced varix = S,V; (3) smooth, with 
varix but with sporadic low ribs on penulti- 
mate and body whorl; these may appear as 
exaggerated growth lines = S +; (4) ribbed 
and with varix, the ribs are numerous (15-18 
on the lower whorls) and pronounced but low 
in profile = R; (5) pronounced high profile ribs, 
few in number on the lower whorls (12-13), 
with varix = R+. Each population consists of 
one phenotypic class only. 

Electrophoresis 

Horizontal starch gel electrophoresis of 
tissue proteins was followed by staining 
for the following 30 loci: AAT-1, AAT-2 (as- 
partate aminotransferase, 2.6.1.1); AK 
(adenosine kinase, 2.7.1.20); AG (aldehyde 
oxidase, 1.2.3.1); ACPH (acid phospha- 
tase, 3.1.3.2); APH (alkaline phosphatase, 
3.1.3.1); CK (creatine kinase, 2.7.3.2); EST-1, 
EST-2, EST-3 (esterase, 3.1.1.1); GDH (glu- 
tamate dehydrogenase, 1.4.1.2); G6PD-1, 
G6PD-2 (glucose-6-phosphate dehydroge- 
nase, 1.1.1.49); GPI (glucose-6-phosphate 
isomerase); ISDH-1, ISDH-2, ISDH-3 (isoci- 
trate dehydrogenase, 1.1.1.42); LDH (L-lac- 
tate dehydrogenase, 1.1.1.42); MDH (malic 
dehydrogenase, 1 .1 .1 .37); ME-1 , ME-2 (malic 
enzyme, 1.1.1.40); MPI (mannose-6-phos- 
phate isomerase, 5.3.1.9); NADD-1 (NADH 
dehydrogenase, 1.6.99.3); 6PGD (phospho- 
gluconate dehydrogenase, 1.1.1.44); PGM-1, 
PGM-2 (phosphoglucomutase, 5.4.2.2); OCT 
(octopine dehydrogenase, 1.5.1.11); SDH-1; 
SDH-2 (sorbitol dehydrogenase, 1.15.1.1) ; 
XDH (xanthine dehydrogenase, 1.1.1.204). 
Procedures are those of Ayala et al. (1 973) as 
modified by Dillon and Davis (1980), Davis 
(1983), Davis et al. (1981, 1988), and most 
recently for Oncomelania, by Davis et al. 
(1994). 

Because the number of snails was limited, 
and because the two groups were studied 
some months apart, it was not possible to 
obtain results for all loci for all populations. In 
comparing the two groups of populations, in- 
sufficient snails were available to fill in miss- 
ing data for some loci and to be absolutely 
certain of homology of scoring among some 
populations. Accordingly, the results are 
given for each group of populations sepa- 
rately before giving the combined data set. 
The combined data set for 14 populations 
involved 25 loci. The following loci were not 
included: AAT-2; ME-2; CK; GDH; ISDH-3. 

Genetic parameters were calculated using 
BIOSYS-1 (Swofford & Selander. 1981). 



POPULATION GENETICS OF ONCOMELANIA HUPENSIS 



135 



TABLE 1 . Populations, localities, and catalog numbers for the fourteen populations of the 
two groups. Localities are listed as they occur west to east. Latitudes and longitudes are 
given. They are provided for the county town when the precise locality in the county is 
not known. Shell sculptural types are as follows: Smooth; Smooth+ = smooth with a few 
low riblets scattered on the last two whorls of some shells, some looking as strong growth 
lines; Ribs+ = ribs very strong, few and high, about 11-13 on the body whorl; Ribbed = 
ribs strong, low but pronounced, many, i.e. some 1 8-1 9 on the body whorl or penultimate 
whorl. 

Group I snails collected in October 1984: 

1. Yunnan Province; Dali County = DA, Fig. 1 

25 44'43"N; 100'7'16"E; ANSP 398317, AI 8327 
shell: smooth; no varix 

2. Sichuan Province; XiChang City = XI, Fig. 1 

26 57'49"N; 102 7'58"E; ANSP 398322; AI 8333 
shell: smooth; no varix 

3. Hubei Province; JianLi County = Jl, Fig. 1 
29"49'N; 112 54'E; ANSP 398320; AI 8330 

shell: ribbed; vahx strong 

4. Jiangxi Province; PengZe County = PZ, Fig. 1 

29 54'N; 116 32'E; ANSP 398321; AI 8331 
shell: ribs+; varix strong 

5. Anhui Province; GuiChi City = GC, Fig. 1 
117 20.6'E; 30 30'N; CIPD 0356; ANSP 398319; A18329 

shell: ribs+; varix strong 

6. Fujian Province; FuQing County = FQ, Fig. 1 
25 43'38"N; 119 24'00"E; ANSP 398317; AI 8332 

shell: smooth; varix strong and wide 

7. Fujian Province; XiaPu County = XP, Fig. 1 
26^'50'11"N; 120'E; ANSP 398323; AI 83333 

shell: smooth; varix strong and wide 
Group II collected in November 1985: 
1(8). Guangxi Province; GuiPing County = GP, Fig. 1 

23 23'27"N; 110 04'42"E; ANSP 375733 
shell: smooth+; varix strong 
2(9). Hubei Province; JiangLing County = JL, Fig. 1 

30 20'57"N: 112 1ГЕ; ANSP 375528 
shell: ribbed; varix strong 

3(10). Hunan Province; YueYang City = YY, Fig. 1 

29 22'52"N; 113 06'00"E; ANSP 375732 
shell: ribs+; varix strong 

4(11). Hubei Province; HanYang County = HY, Fig. 1 

30'34'46"N; 114 01'06"E; ANSP 375731 

shell: ribs+; varix strong 
5(12). Anhui Province; TongLing County/City = TL, Fig. 1 

30 12'35"N; 116 05'27"E; ANSP 375730 
shell: ribs+; varix strong 

6(13). Anhui Province; NingGuo County = NG, Fig. 1 

30 22'23"N; 118 58'21"E; ANSP 37573 

shell: smooth; varix strong 
7(14). Zhejiang Province; Chang Xing County = CX, Fig. 1 

near Anji; 31 01'35"N; 119°54'29°E; ANSP 375729 

shell: smooth; no varix 



Hardy-Weinberg equilibrium was analyzed 
for all polymorphic loci. Nei's (1978) genetic 
distance and Cavalli-Sforza & Edwards' 
(1967) arc distance were calculated and 
phenograms constructed using the UPGMA 
method. Homology of alleles at certain loci 
could not be rechecked because of lack of 
specimens, and therefore Nei's (1978) unbi- 



ased minimum distance (mD) was used so as 
not to inflate D due to possible error. Un- 
rooted trees based on mD were also con- 
structed using the FITCH program of PHYLIP 
version 3.4 (Felsenstein, 1989). This phyloge- 
netic analysis program does not assume 
equal rates of evolution. Twenty repetitions of 
FITCH were run with randomized input order 



136 



DAVIS, ZHANG, GUO & SPOLSKY 




FIG. 1. Map of localities in southern China. West to east: DA = Dali; XI = XiChang; GP = GuiPing; JL 
JiangLing; J! = JianLi; YY = YueYang; HY = HanYang; PZ = PengZe; GC = GuiChi; TL = TongUng; NG 
NingGuo; FQ = FuQing; OX = ChangXing; XP =^ XiaPu. 



and optimization by global branch rearrange- 
ment. 



RESULTS 

Indices of genetic variability are given in 
Table 2. Mean heterozygosity is low, with 
means ranging from 0.008 to 0.093 (1 .1 to 1 .6 
alleles per locus). The percentage of poly- 
morphic loci ranged from 4.0 to 28.0. The 
lowest levels (4.0 to 8.0) involved smooth- 
shelled populations from Fujian and Sichuan 
provinces in the west, and from Zhejiang 
Province in the east. The mean value for 
smooth-shelled populations was 9.3 ± 6.0 
(4.0-20.0; N = 6). The highest levels (20.0 to 
28.0) involved ribbed snails from HutDei, An- 
hui, and Jiangxi provinces. The percentage of 
polymorphic loci among ribbed snails was 
20.6 ±4.7 (16-28; N = 7). 

In the analysis of the seven populations in 
group I, allele frequencies for 29 loci involving 
67 alleles are given in Table 3. Nei's D and 
arc distances are given in Table 4. Invariant 
loci and loci with fixed alternative alleles are 



given in Table 5. Phenograms based on these 
distances are given in Figure 6. 

Group I populations represent highly diver- 
gent locations in six different provinces from 
Yunnan to Jiangxi provinces in the interior, 
and from Fujian Province on the coast. Nei's 
D ranges from 0.107 (close geography and 
shell type: Yunnan and Sichuan: smooth 
shells) to 0.346 (Fujian smooth shell type vs. 
Jiangxi ribbed shell type). The mean D was 
0.241 ± 0.066. The corresponding value for 
arc distance is 0.457 ± 0.059 (range of 
0.314—0.538). 

Results from group II are given in Tables 6 
and 7 involving 60 alleles at 28 loci. Nei's D 
averaged 0.234 ± 0.095 (range of 0.089 to 
0.382); arc D averaged 0.440 ± 0.087 (range 
of 0.291 to 0.559). Corresponding pheno- 
grams are given in Figure 7. 

Nine loci were monomorphic in the first 
group, 12 in the second (Table 5). One locus 
in each group was invariant except for one 
population; thus there were 19 and 14 infor- 
mative loci, respectively. There were fixed 
differences at eight loci in each group (Table 
5). There were minor deviations from Hardy- 



POPULATION GENETICS OF ONCOMELANIA HUPENSIS 



137 




FIG. 2. Localities as in Fig. 1 , but showing the distribution of shell types. Relative shell sizes are as shown. 



Weinberg equilibrium in both groups of pop- 
ulations (Table 8). In the first group, these 
involved four populations, five of 25 polymor- 
phic loci (summed over all populations), and 
primarily reflected heterozygote deficiency. 
In the second group, deviations occurred in- 
five populations at three of 28 polymorphic 
loci; the esterase-2 locus was involved in 
three of the five populations. Grouping pop- 
ulations from west to east along the Yangtze 
River drainage, Nei's D averaged as follows: 
Yunnan-Sichuan, 0.107 (group I); Hubei- 
Hunan, 0.089—0.102 (group II, N = 3); Anhui, 
0.231 (group II, N = 2). 

For the combined data-set, the matrix of 
Nei's (1978) unbiased minimum distance is 
given in Table 9. The UPGMA phenogram 
based on these data is given in Figure 8. The 
greatest Nei's minimum distance was 0.453 
(between Gui Ping and Fu Qing). In the phe- 
nogram, the populations are grouped in two 
major clusters. The upper cluster is, with 
three exceptions, a smooth-shelled cluster 
with shells having no varix (Dali, Chang Xing, 
Xi Chang) at the top; and the Fujian Province 
populations with smooth shells and low wide 
varix (Fu Qing, Xia Pu) at the bottom. Three 



populations seem out of place because they 
have ribbed shells: Tong Ling, Jian Li, and 
Gui Chi. Tong Ling has relatively low genetic 
distances to the Yunnan (Dali) and Sichuan 
(Xi Chang) populations and the lowest ge- 
netic distance (mD = 0.092) to the Zhejiang 
population (Table 9). The presence of ribbed 
shells in these snails, which are genetically 
closest to smooth-shelled populations, sug- 
gests the possibility that this is a hybrid pop- 
ulation. The same might be the case for the 
Jian Li and Gui Chi populations, which also 
have closer genetic affinity with the upper 
section taxa of the phenogram. 

The lower cluster, with an average pairwise 
mD of 0.160 ± 0.07, is one characterized by 
populations with ribbed shells, except for the 
Ning Guo (Anhui) and the Gui Ping (Guangxi) 
smooth-shelled populations. These excep- 
tions will be discussed later. In sum, popula- 
tions clustered in Figure 8 appear to repre- 
sent three genetically cohesive groups: the 
Yunnan, Sichuan, and Zhejiang smooth- 
shelled populations with no varix; the two 
smooth-shelled Fujian populations with low 
wide shells and a low wide varix; a cohesive 
group of ribbed-shelled populations, which 



138 



DAVIS, ZHANG, GUO & SPOLSKY 




FIG. 3. Examples of shells from six localities: A. Dali, Yunnan Province = Oncomelania hupensis robertsoni: 
B. XiChang, Sichuan Province = O. h. robertsoni: С ChangXing, Zhejiang Province = O. h. robertsoni: D. 
FuQing, Fujian Province = O. Ii. tangi: E. XiaPu, Fujian Province = O. ii. tangi: F. NingGuo, Anhui Province 
= O. In. hupensis (fausti form). The shell at the top left is 6.0 mm; others are printed to the same scale. 



POPULATION GENETICS OF ONCOMELANIA HUPENSIS 



139 




FIG. 4. Examples of shells from six localities: A. GuiPing, Guangxi Province = O. hupensis guangxiensis; B. 
JianLi, Hubei Province = O. h. hupensis; С JianLing, Hubei Province = O. h. hupensis; D. PengZe, Jiangxi 
Province = O. h. hupensis; E. GuiChi, Anhui Province = O. h. hupensis; F. YueYang, Hunan Province = O. 
h. hupensis. The shell at the top left is 6.69 mm long; others are printed to the same scale. 



140 



DAVIS, ZHANG, GUO & SPOLSKY 




FIG. 5. Examples of shells from two localities: A. TongLIng, Anhui Province = Oncomelania hupensis 
hupensis] B. HanYang, Hubei Province = O. h. hupensis. The top left shell is 7.75 mm long; others are 
printed to the same scale. 



includes two exceptions that will be dis- 
cussed later. In addition, there are three pos- 
sible hybrid populations in the upper cluster. 
The general topology of the UPGMA pheno- 
gram is confirmed by FITCH analyses. Figure 
9 gives the best unrooted FITCH tree (sum of 
squares = 2.165); the 20 repetitions pro- 
duced only four unique trees, with three clear 
groupings in each case: Yunnan-Sichuan- 
Zhejiang (Dali group), Fu Qing — Xia Pu (Fujian 
group), and a mainly ribbed group of six pop- 
ulations (Han Yang, Gui Ping, Yue Yang, 
Peng Ze, Jiang Ling, and Ning Guo). The dif- 
ferences in the four FITCH trees occurred 
only in relative placement and branch lengths 
of the three possibly hybrid populations; in all 
cases, however, these three populations 
were positioned between the two smooth- 
shelled groups on the one hand and the 
ribbed group on the other. The former two 
groups are found in the upper cluster in the 
UPGMA phenogram; the latter group corre- 
sponds exactly to the lower cluster in the UP- 
GMA tree. Thus, the differences between the 
UPGMA and FITCH analyses lie mainly in the 



placement of the three putative hybrid pop- 
ulations. 

Genetic Distance, Shell Sculpture and 
Geographic Distance. 

Pairwise comparisons among populations 
on the basis of Nei's minimum D from the 
smallest value to 0.156, along with the shell 
type, are given in Table 10. The value of 
0.156 was arbitrarily chosen to represent the 
upper limit of divergence that one might the- 
oretically expect between populations based 
on a number of studies of diverse taxa (re- 
viewed in Ayala and Aquadro, 1982). It is 
clear, even without doing a Mantel test (Rice, 
1989), that there is no correlation between 
geographic distance and genetic distance 
when one considers all 14 populations. The 
two farthest separated populations have the 
lowest genetic distance (mD = 0.007 over 
>2, 000km), whereas closest neighbors have 
an mD of 0.204 at 44 km, and of 0.339 at 72 
km. This lack of correlation provided the pre- 
liminary indication that the set of 14 popula- 



POPULATION GENETICS OF ONCOMELANIA HUPENSIS 



141 



TABLE 2. Genetic variability at 25 loci for all 14 populations studied. 











Mean Heterozygosity 




Mean sample 


Mean no. 










size per 


alleles per 


% loci 


direct- 


Hdywbg 


Population 


locus 


locus 


polymorphic 


count 


expected 


1. Dali (Yunnan) 


30.0 


1.1 


12.0 


0.028 


0.035 




(0.0) 


(0.1) 




(0.017) 


(0.021) 


2. FuQing (Fujian) 


25.0 


1.1 


8.0 


0.008 


0.013 




(0.0) 


(0.1) 




(0.017) 


(0.010) 


3. GuiChi (Anhui) 


14.9 


1.4 


24.0 


0.077 


0.093 




(0.1) 


(0.2) 




(0.036) 


(0.039) 


4. JianLi (Hubei) 


15.0 


1.4 


20.0 


0.045 


0.082 




(0.0) 


(0.2) 




(0.021) 


(0.039) 


5. PengZhe (JiangXi) 


25.0 


1.6 


28.0 


0.093 


0.110 




(0.0) 


(0.2) 




(0.036) 


(0.043) 


6. XiChang (Sichuan) 


16.2 


1.0 


4.0 


0.008 


0.022 




(1.0) 


(0.0) 




(0.008) 


(0.022) 


7. XiaPu (Fujian) 


25.0 


1.1 


8.0 


0.026 


0.022 




(0.0) 


(0.1) 




(0.020) 


(0.017) 


8. ChangXing (Zhejiang) 


25.0 


1.0 


4.0 


0.010 


0.018 




(0.0) 


(0.0) 




(0.010) 


(0.018) 


9. TongLing (Anhui) 


25.0 


1.5 


16.0 


0.064 


0.082 




(0.0) 


(0.2) 




(0.032) 


(0.040) 


10. JiangLing (Hubei) 


25.0 


1.5 


20.0 


0.064 


0.082 




(0.0) 


(0.2) 




(0.032) 


(0.040) 


11. YueYang (Hunan) 


25.0 


1.4 


16.0 


0.085 


0.082 




(0.0) 


(0.2) 




(0.041) 


(0.039) 


12. GuiPing (GuangXi) 


25.0 


1.1 


12.0 


0.074 


0.061 




(0.0) 


(0.1) 




(0.041) 


(0.034) 


13. NingGuo (Anhui) 


25.0 


1.2 


20.0 


0.074 


0.055 




(0.0) 


(0.1) 




(0.044) 


(0.028) 


14. HanYang (Hubei) 


25.0 


1.4 


20.0 


0.070 


0.073 




(0.0) 


(0.2) 




(0.035) 


(0.035) 



tions is not a valid grouping, and suggested 
the existence of discrete subgroups of O. hu- 
pensis. 

In Table 1 1 are given pairwise comparisons 
between populations listed by an increasing 
value of D fronn Tables 3 and 7. Crisscrossing 
through southern China the values gradually 
increase by increments of 0.020 ± 0.01 (N = 
15). There are no big gaps to suggest a 
change from population groupings to dis- 
crete species. 

However, when populations are separated 
into groups based on chonchological and 
geographic criteria (Table 12), significant dif- 
ferences are evident among the different 
groups of populations. The Dali group of 
three populations with smooth shells without 
varix have a small average distance among 
them (0.081). A relatively small distance is 
found between the two Fujian populations 
with smooth shells but with a low, wide varix 
(0.154). Distances jump to >0.200 for inter- 
group comparisons of smooth-shelled popu- 
lations. 

When all ribbed shells are compared, the 



average distance is 0.204 ± 0.085; one stan- 
dard deviation ranges from 0.119 to 0.289. 
However, if one excludes the three putative 
hybrid populations, the remaining six popu- 
lations form a genetically cohesive group; 
this group includes two smooth-shelled pop- 
ulations where shells have a varix. This pre- 
dominantly ribbed-shelled set of populations 
has a much lower average pairwise distance, 
0.160. This distance is similar to the interpop- 
ulational differences within the Fujian group 
(0.154) and to the range of the Dali group 
(0.007 to 0.127). Thus, there are no signifi- 
cant within-group differences in distances 
between the coherent ribbed-shelled group 
of six and the two major smooth-shelled 
groups, Dali and Fujian. There is a clear gap 
between interpopulation distances within 
groups (Dali, Fujian, and ribbed; mD < 0.160) 
and intergroup distances between smooth 
and ribbed populations (mD > 0.300). For the 
three ribbed, possibly hybrid populations 
(Tong Ling, Gui Chi, Jiang Li), comparisons of 
each to the Dali group, the Fujian group, the 



142 



DAVIS, ZHANG, GUO & SPOLSKY 



TABLE 3. Allele frequencies for seven populations of Oncomelania hupensis from throughout China 
(group I). 29 loci; 67 alleles. 'Same number of individuals from each population at all loci. There were 
nine invariant loci; see Table 5. AAT-2 was not detected in XiChang, population 6. 











POPULATION 








Locus 


DALI 


FUQING 


GUICHI 


JIANLI 


PENGZE 


XICHANG 


XIAPU 


(N)* 


30 


25 


15 


15 


25 


18 


25 


AAT-1 
















A 


1.0 


0.0 


0.97 


1.0 


0.0 


0.0 


1.0 


В 


0.0 


1.0 


0.0 


0.0 


1.0 


1.0 


0.0 


С 


0.0 


0.0 


0.03 


0.0 


0.0 


0.0 


0.0 


AAT-2 
















A 


1.0 


1.0 


0.87 


1.0 


1.0 


— 


0.74 


В 


0.0 


0.0 


0.13 


0.0 


0.0 


— 


0.26 


ACPH 
















A 


0.0 


0.0 


1.0 


0.0 


0.0 


0.0 


0.0 


В 


1.0 


1.0 


0.0 


1.0 


1.0 


1.0 


1.0 


AK 
















A 


0.0 


0.0 


1.0 


0.0 


0.0 


0.0 


0.0 


В 


1.0 


1.0 


0.0 


1.0 


1.0 


1.0 


1.0 


APH 
















A 


1.0 


1.0 


1.0 


0.0 


1.0 


1.0 


1.0 


В 


0.0 


0.0 


0.0 


1.0 


0.0 


0.0 


0.0 


EST-1 
















A 


1.0 


0.86 


1.0 


1.0 


0.96 


0.0 


0.0 


В 


0.0 


0.0 


0.0 


0.0 


0.02 


0.50 


0.0 


С 


0.0 


0.0 


0.0 


0.0 


0.0 


0.50 


0.0 


D 


0.0 


0.14 


0.0 


0.0 


0.02 


0.0 


1.0 


EST-2 
















A 


1.0 


1.0 


0.56 


0.43 


0.78 


1.0 


0.72 


В 


0.0 


0.0 


0.40 


0.30 


0.18 


0.0 


0.0 


С 


0.0 


0.0 


0.03 


0.17 


0.04 


0.0 


0.28 


D 


0.0 


0.0 


0.0 


0.10 


0.0 


0.0 


0.0 


EST-3 
















A 


1.0 


0.0 


0.92 


1.0 


1.0 


1.0 


1.0 


В 


0.0 


1.0 


0.0 


0.0 


0.0 


0.0 


0.0 


С 


0.0 


0.0 


0.08 


0.0 


0.0 


0.0 


0.0 


G6PD-2 
















A 


0.97 


1.0 


1.0 


1.0 


1.0 


1.0 


1.0 


В 


0.03 


0.0 


0.0 


0.0 


0.0 


0.0 


0.0 


GPI 
















A 


0.0 


0.0 


0.57 


0.90 


0.70 


1.0 


0.0 


В 


0.0 


1.0 


0.40 


0.07 


0.28 


0.0 


1.0 


С 


0.0 


0.0 


0.03 


0.0 


0.0 


0.0 


0.0 


D 


0.93 


0.0 


0.0 


0.0 


0.0 


0.0 


0.0 


E 


0.07 


0.0 


0.0 


0.0 


0.0 


0.0 


0.0 


F 


0.0 


0.0 


0.0 


0.03 


0.02 


0.0 


0.0 


LDH 
















A 


1.0 


1.0 


1.0 


1.0 


0.0 


1.0 


1.0 


В 


0.0 


0.0 


0.0 


0.0 


1.0 


0.0 


0.0 


MDH 
















A 


0.0 


1.0 


1.0 


1.0 


1.0 


0.0 


1.0 


В 


1.0 


0.0 


0.0 


0.0 


0.0 


1.0 


0.0 


NADD 
















A 


1.0 


1.0 


1.0 


1.0 


0.0 


1.0 


1.0 


В 


0.0 


0.0 


0.0 


0.0 


1.0 


0.0 


0.0 



POPULATION GENETICS OF ONCOMELANIA HUPENSIS 



143 



TABLE 3. (Continued) 











POPULÛ.TION 








Locus 


DALI 


FUQING 


GUICHI 


JIANLI 


PENGZE 


XICHANG 


XIAPU 


OCT 
















A 


1.0 


1.0 


0.70 


0.57 


0.32 


1.0 


1.0 


В 


0.0 


0.0 


0.0 


0.0 


0.24 


0.0 


0.0 


С 


0.0 


0.0 


0.0 


0.0 


0.04 


0.0 


0.0 


D 


0.0 


0.0 


0.30 


0.30 


0.26 


0.0 


0.0 


E 


0.0 


0.0 


0.0 


0.13 


0.12 


0.0 


0.0 


F 


0.0 


0.0 


0.0 


0.0 


0.02 


0.0 


0.0 


6PGD 
















A 


1.0 


1.0 


0.0 


1.0 


0.0 


1.0 


1.0 


В 


0.0 


0.0 


1.0 


0.0 


1.0 


0.0 


0.0 


PGM-1 
















A 


0.72 


0.0 


0.07 


0.0 


0.04 


1.0 


0.0 


В 


0.28 


1.0 


0.53 


0.77 


0.62 


0.0 


1.0 


С 


0.0 


0.0 


0.37 


0.20 


0.34 


0.0 


0.0 


D 


0.0 


0.0 


0.03 


0.03 


0.0 


0.0 


0.0 


PGM-2 
















A 


1.0 


0.0 


1.0 


1.0 


0.90 


1.0 


0.08 


В 


0.0 


1.0 


0.0 


0.0 


0.02 


0.0 


0.93 


С 


0.0 


0.0 


0.0 


0.0 


0.08 


0.0 


0.0 


SDH-1 
















A 


0.82 


0.94 


1.0 


0.0 


0.72 


1.0 


1.0 


В 


0.18 


0.06 


0.0 


0.90 


0.0 


0.0 


0.0 


С 


0.0 


0.0 


0.0 


0.10 


0.0 


0.0 


0.0 


D 


0.0 


0.0 


0.0 


0.0 


0.28 


0.0 


0.0 


XDH 
















A 


1.0 


1.0 


1.0 


1.0 


0.0 


1.0 


1.0 


В 


0.0 


0.0 


0.0 


0.0 


1.0 


0.0 


0.0 



TABLE 4. Pairwise genetic distances among the seven populations of group I; Nei's (1978) D below the 
diagonal; arc D above the diagonal. The iow/er set includes the AAT-2 locus, which was not scorable for 
XiChang and therefore excluded from the upper set. 



POPUI^TION 


DA 


FQ 


GC 


Jl 


PZ 


XI 


XP 


Dali 


— 


0.443 


0.456 


0.402 


0.538 


0.339 


0.392 


FuQing 


0.223 


— 


0.499 


0.466 


0.503 


0.460 


0.314 


GuiChi 


0.221 


0.287 


— 


0.436 


0.482 


0.510 


0.448 


JianLi 


0.171 


0.255 


0.217 


— 


0.513 


0.483 


0.417 


PengZe 


0.334 


0.302 


0.278 


0.312 


— 


0.515 


0.521 


XiChang 


0.107 


0.227 


0.292 


0.244 


0.301 


— 


0.455 


XiaPu 


0.176 


0.108 


0.233 


0.200 


0.346 


0.230 


— 


POPULATION 


DA 


FQ 


GC 


Jl 


PZ 


XI 


XP 


Dali 


— 


0.395 


0.411 


0.364 


0.481 


— 


0.358 


FuQing 


0.214 


— 


0.449 


0.419 


0.452 


— 


0.289 


GuiChi 


0.214 


0.277 


— 


0.391 


0.432 


— 


0.404 


JianLi 


0.164 


0.245 


0.210 


— 


0.456 


— 


0.381 


PengZe 


0.320 


0.289 


0.268 


0.298 


— 


— 


0.473 


XiChang 


— 


— 


— 


— 


— 


— 


— 


XiaPu 


0.173 


0.107 


0.227 


0.197 


0.337 


— 


— 



ribbed group of five, and separately the Ning 
Quo population, show that in each case, the 
putative hybrid population is genetically clos- 



est to the Dali group (Dali group — Tong Ling, 
0.116; Dali group— Jiang Li, 0.189; Dali 
group — Gui Chi, 0.227). These three excep- 



144 



DAVIS, ZHANG, GUO & SPOLSKY 



TABLE 5. Loci fixed for a single allele or having 
alternative alleles 



Invariant loci 


Group 1 


Group 2 


АО 


X 


X 


AK 


— 


X 


APH 


— 


X 


CK 


X 


X 


EST-3 


— 


X 


GDH 


X 


X 


G6PD-2 


— 


X 


ISDH-1 


X 


X 


ISDH-2 


X 


— 


ME-1 


X 


X 


ME-2 


X 


X 


MP! 


X 


X 


SDH-1 


— 


X 


SDH-2 


X 


X 


TOTAL 


9 


12 


Invariant except populat 


ion 




G6PD-2 


1 (DA) 


— 


EST-1 


— 


10 (JL) 


Fixed for alternative alleles 




AAT-1 


— 


X 


ACPH 


X 


X 


AK 


X 


— 


APH 


X 


— 


ISDH-2 


— 


X 


LDH 


X 


X 


MDH 


X 


— 


ME-2 


— 


X 


NADD-1 


X 


X 


6PGD 


X 


X 


XDH 


X 


X 


TOTAL 


8 


8 


Alternative allele except 


population 




AAT-1 


3(GC) 




EST-3 


3(GC) 


— 


MDH 


— 


8(JL) 



tional populations are also fairly closely re- 
lated to each other (average mD 0.187), but 
not clearly to any other group. 



DISCUSSION 

Population Genetics 

Populations of Oncomelania studied here 
are not unusual in having few alleles per lo- 
cus (1 .0 to 1 .6), a low mean heterozygosity 
(0.008 to 0.036), and low percentage of poly- 
morphic loci (4 to 28). In a previous study of 
Oncomelania from China and the Philippines, 
Woodruff et al. (1988) found 16 polymorphic 
loci among 21 loci studied, with 1.8 to 2.1 
alleles per locus, in two populations from Gui 



Chi in Anhui Province; mean heterozygosity 
was 0.19 to 0.20, and the percentage of poly- 
morphic loci ranged from 52 to 62. The major 
difference between these two studies of On- 
comelania is that in this study we had results 
from 29 loci. Had we studied only 21 loci. Gui 
Chi of our study would have had 33% poly- 
morphic loci rather than 24%. This, however, 
is not the only source of discrepancy. Wood- 
ruff et al. (1988) reported polymorphism at 
three loci where we found none: LAP, ACP, 
ME; in addition, they had a polymorphism at 
PEP locus we did not study. Even with ex- 
tensive additional screening of our Gui Chi 
population (250 additional individuals; 38 
loci), the number of polymorphic loci still re- 
mains relatively low, 44%). 

The results found in our study were similar 
to those found in sister taxa of rissoacean 
snails in the genus Hydrobia (Hydrobiidae): 
Davis et al. (1988, 1989), one species, six 
populations (30 loci); Haase (1993), three 
species (25 loci); and in Truncatella: Rosen- 
berg (1989), five species (19 loci), one spe- 
cies with four populations. In the Truncatella 
study, four populations had a mean heterozy- 
gosity above 0.036 (0.037 to 0.077). How- 
ever, the 0.077 value derived from a mean 
sample size of 5.3 snails analyzed per locus. 
The mean number of alleles per locus varied 
from 1.1 to 1.4; mean heterozygosity varied 
from 0.006 to 0.077; the percentage of poly- 
morphic loci varied from 5.3 to 31 .6. In sum- 
mary, the Oncomelania populations studied 
here are normally outbreeding rissoacean- 
grade snails with an apparent usual pattern 
of low heterozygosity and low percentage of 
polymorphic loci. 

Genetic distance and 
taxonomic discrimination 

Where do populations stop and higher taxa 
begin? This topic was reviewed extensively 
by Davis (1994) with particular reference to 
Oncomelania hupensis. Large genetic dis- 
tances by themselves do not serve to define 
species. There is no magical cut off point be- 
low which are populations and above which 
are species. We have demonstrated the 
gradual rise of Nei's D to the 0.400 level in 
pairwise comparisons of populations across 
China, but again, this does not hold if one 
excludes the three candidate hybrid popula- 
tions. We documented the very great inter- 
population variance in Nei's minimal D for the 
ribbed populations traditionally classified as 



POPULATION GENETICS OF ONCOMELANIA HUPENSIS 



145 



NEI'S 1978 D 



CHANG XING 


ZHEJIANG 


S 


NV 


TONG LING. 


ANHUI 


R< 


V 


JIANG LING. 


HUBEI 


R 


V 


YUE VANG. 


HUNAN 


R* 


V 


HAN YANG, 


HUBEI 


R» 


V 


GUI PING, 


GUANGXI 


S4 


V 


NING GUO, 


ANHUI 


S 


V 



^ 



CHANG XING . 


ZHEJIANG 


S 


NV 


TONG LING, 


ANHUI 


R» 


V 


JIANG LING, 


HUBEI 


R 


V 


YUE YANG. 


HUNAN 


R« 


V 


HAN YANG , 


HUBEI 


R,» 


V 


GUI PING . 


GUANGXI 


S* 


V 


NING GUO, 


ANHUI 


S 


V 



FIG. 6. UPGMA derived phenograms based on Nei's 1978 D and Cavalli-Sforza's Arc D for group I 
populations. 



Oncomelania hupensis hupensis (range of 
0.048 to 0.324). 

Woodruff et al. (1988) showed that On- 
comelania hupensis quadrasi populations 
fronn the Philippines differed fronn Oncomel- 
ania hupensis hupensis from China by a D of 
0.62 ± 0.04 and on this basis, invoking the 
"evolutionary species concept," stated that 
two species rather than subspecies were in- 
volved. On the other hand, Davis (1994) 
noted that the land snail Cepaea nemoralis 
introduced from Europe to the southern 
U.S.A. differed by a D of 0.631 between con- 
tinents (Johnson et al., 1984) and that a pop- 
ulation near Pavia, Italy, differed from another 
from Florence, Italy, by D = 0.391. This spe- 
cies, used in various paradigms in evolution, 
is well known for geographic variation in shell 
polymorphisms and allozymes. Quoting 
Johnson et al. (1984), "The decoupling of ge- 
netic distance from speciation emphasizes 
the limitations of viewing the process of spe- 
ciation solely in genetic terms" (see also 
Stine, 1989 and Murray et al., 1991). 

The large genetic distances in our and the 
Woodruff studies are caused by six or more 
loci with alternative allele(s). Alternative alle- 
les in allopatric populations are largely re- 
sponsible for the results seized upon by 
Woodruff et al. (1 988) to defend an evolution- 



ary or phylogenetic species concept. But is 
this justified? 

Species concepts and Oncomelania 

In describing new species, and especially 
in applying molecular genetic data in the pro- 
cess, one must commit to a species concept 
and be prepared to defend that concept. 
Davis (1 994) reviewed this topic in arguing for 
Templeton's (1989) "cohesion" model, 
which includes the biological species con- 
cept whenever it applies as well as Patter- 
son's (1985) recognition concept. The cohe- 
sion model integrates population genetics 
and ecology with standard studies of mor- 
phology. The concept can be applied to all 
organisms from outbreeders to syngameons 
or parthogenetic organisms. 

Among populations of Oncomelania hu- 
pensis one finds considerable cohesion! 
Given that each morphological character is 
controlled by one to several genes, morpho- 
logical distance is a measure of relative ge- 
netic distance. Aside from size and a few 
shell characters, the allopatric populations of 
this species are qualitatively the same. Ac- 
cordingly, the relative genetic divergence ex- 
pressed in morphology is extremely low. Re- 
productive cohesion is also large. Allopatric 



146 



DAVIS, ZHANG, GUO & SPOLSKY 



TABLE 6. Allele frequencies for seven populations of Oncomelania hupensis from south-central China 
(group II). 28 loci (no CK: GDH). N = 25 for all populations, all loci. There were 12 invariant loci; see 
Table 5. 











Population 








Locus 


ChangXing 


TongLing 


JiangLing 


YueYang 


GuiPing 


NingGuo 


HanYang 


AAT-1 
















A 


1.0 


1.0 


0.0 


1.0 


1.0 


0.0 


1.0 


В 


0.0 


0.0 


1.0 


0.0 


0.0 


0.0 


0.0 


С 


0.0 


0.0 


0.0 


0.0 


0.0 


1.0 


0.0 


AAT-2 
A 


1.0 


1.0 


0.92 


0.96 


1.0 


1.0 


1.0 


В 


0.0 


0.0 


0.02 


0.0 


0.0 


0.0 


0.0 


С 


0.0 


0.0 


0.06 


0.0 


0.0 


0.0 


0.0 


D 


0.0 


0.0 


0.0 


0.04 


0.0 


0.0 


0.0 


ACPH 
















A 


0.0 


0.0 


0.0 


0.0 


1.0 


0.0 


0.0 


В 


1.0 


1.0 


1.0 


1.0 


0.0 


1.0 


1.0 


EST-1 
















A 


1.0 


1.0 


0.44 


1.0 


1.0 


1.0 


1.0 


В 


0.0 


0.0 


0.44 


0.0 


0.0 


0.0 


0.0 


С 


0.0 


0.0 


0.0 


0.0 


0.0 


0.0 


0.0 


D 


0.0 


0.0 


0.12 


0.0 


0.0 


0.0 


0.0 


EST-2 
















A 


1.0 


0.46 


1.0 


0.46 


0.46 


0.50 


0.78 


В 


0.0 


0.42 


0.0 


0.46 


0.0 


0.50 


0.0 


С 


0.0 


0.12 


0.0 


0.08 


0.54 


0.0 


0.22 


GPi 
















A 


0.0 


0.80 


0.70 


0.72 


0.48 


0.38 


0.80 


В 


0.0 


0.0 


0.14 


0.16 


0.0 


0.62 


0.20 


С 


0.0 


0.02 


0.0 


0.0 


0.0 


0.0 


0.0 


D 


1.0 


0.02 


0.04 


0.04 


0.0 


0.0 


0.0 


E 


0.0 


0.10 


0.02 


0.02 


0.0 


0.0 


0.0 


F 


0.0 


0.02 


0.04 


0.02 


0.0 


0.0 


0.0 


G 


0.0 


0.02 


0.06 


0.04 


0.52 


0.0 


0.0 


ISDH-2 
















A 


1.0 


1.0 


0.0 


0.0 


0.0 


0.0 


0.0 


В 


0.0 


0.0 


1.0 


1.0 


1.0 


1.0 


1.0 


LDH 
















A 


1.0 


1.0 


0.0 


0.0 


0.0 


1.0 


0.0 


G 


0.0 


0.0 


1.0 


1.0 


0.0 


0.0 


1.0 


D 


0.0 


0.0 


0.0 


0.0 


1.0 


0.0 


0.0 


MDH 
















A 


0.0 


0.0 


0.98 


1.0 


0.0 


0.0 


0.0 


В 


1.0 


1.0 


0.0 


0.0 


1.0 


1.0 


1.0 


С 


0.0 


0.0 


0.02 


0.0 


0.0 


0.0 


0.0 


ME-2 
















A 


1.0 


1.0 


1.0 


0.0 


0.0 


1.0 


1.0 


В 


0.0 


0.0 


0.0 


1.0 


1.0 


0.0 


0.0 


NADD 
















A 


1.0 


1.0 


0.0 


0.0 


0,0 


0.0 


0.0 


В 


0.0 


0.0 


1.0 


1.0 


1.0 


0.0 


1.0 


С 


0.0 


0.0 


0.0 


0.0 


0.0 


1.0 


0.0 


OCT 
















A 


1.0 


0.54 


0.40 


0.34 


1.0 


0.88 


0.56 


В 


0.0 


0.14 


0.0 


0.06 


0.0 


0.08 


0.04 


С 


0.0 


0.0 


0.0 


0.0 


0.0 


0.04 


0.0 


D 


0.0 


0.26 


0.56 


0.60 


0.0 


0.0 


0.38 


E 


0.0 


0.06 


0.04 


0.0 


0.0 


0.0 


0.02 



POPUIJ\TION GENETICS OF ONCOMELANIA HUPENSIS 



147 



TABLE 6. (Continued) 













Population 








Locus 


ChangXing 


TongLing 


JiangLing 


YueYang 


GuiPing 


NingGuo 


HanYang 


6PGD 


















A 


1.0 




1.0 


0.0 


0.0 


0.0 


0.0 


0.0 


В 


0.0 




0.0 


1.0 


1.0 


1.0 


1.0 


1.0 


PGM-1 


















A 


0.32 


0.0 


0.0 


0.0 


0.0 


0.06 


0.02 


В 


0.68 


0.64 


0.52 


0.62 


0.46 


0.94 


0.44 


С 


0.0 




0.34 


0.44 


0.38 


0.54 


0.0 


0.50 


D 


0.0 




0.02 


0.04 


0.0 


0.0 


0.0 


0.02 


E 


0.0 




0.0 


0.0 


0.0 


0.0 


0.0 


0.02 


PGM-2 


















A 


1.0 




1.0 


1.0 


1.0 


1.0 


0.02 


0.98 


В 


0.0 




0.0 


0.0 


0.0 


0.0 


0.98 


0.02 


XDH 


















A 


1.0 




0.0 


0.0 


0.0 


0.0 


0.0 


0.0 


В 


0.0 




1.0 


1.0 


1.0 


1.0 


1.0 


1.0 


TABLE 7. 


Matrices of genetic distances for group 


II populations. 


Nei's (1978) 


D is given 


above the 


diagonal; arc D below the diagonal. 












Population 




OX 


TL 


JL 


YY 


GP 


NG 


HY 


ChangXing 




— 


0.089 


0.381 


0.382 


0.364 


0.301 


0.264 


TongLing 




0.306 


— 


0.293 


0.267 


0.286 


0.231 


0.175 


JiangLing 




0.559 


0.492 


— 


0.102 


0.261 


0.263 


0.093 


YueYang 




0.558 


0.470 


0.310 


— 


0.155 


0.287 


0.089 


GuiPing 




0.556 


0.490 


0.468 


0.373 


— 


0.296 


0.140 


NingGuo 




0.506 


0.448 


0.469 


0.483 


0.506 


— 


0.193 


HanYang 




0.487 


0.397 


0.302 


0.291 


0.360 


0.403 


— 



populations from the Philippines, Japan, 
China can readily interbreed and produce vi- 
able Fi, F2 Fr, generations (reviewed in 
Davis, 1980, 1981). Thus, there is no barrier 
to reproduction; clearly, allozymic differenti- 
ation does not impinge on overall genetic co- 
hesiveness. It appears that gene divergence, 
as seen in allozymes, can change relatively 
rapidly in Oncomelania hupensis, while over- 
all morphological and breeding system rec- 
ognition patterns do not. 

Because the fundamental niche parame- 
ters for allopatric populations of the species 
are the same (van der Schalle and Davis, 
1968; Davis, 1971), the populations are de- 
mographically exchangeable. Behavior is the 
same for all populations, whether from Ja- 
pan, the Philippines or China; that is these 
snails climb upward. In dry periods, they can 
be found cemented to stone walls bounding 
canals or, in the Yangtze flood plain, a meter 
or more up on tree trunks. All populations lay 
their eggs singly, each coated with fine mud. 



Species of Oncomelania 

In contrast to the biological and ecologi- 
cal cohesion among populations of On- 
comelania hupensis, there is considerable 
disruption between the two recognized spe- 
cies of Oncomelania: O. hupensis and O. 
minima (Bartsch, 1936a). Oncomelania min- 
ima comes from northwestern Honshu, Ja- 
pan. The type locality is the Noto Peninsula, 
Ishikawa Prefecture. The species are readily 
distinguished by differences in shell morphol- 
ogy, genital and gill anatomy, and ecology 
(Davis, 1971). Oncomelania minima can be 
amphibious, as is O. hupensis, but the former 
is abundant on sticks, leaves, rocks in a nar- 
row mountain stream. Oncomelania minima 
is also abundant on rock slabs over which 
there was a great amount of water seepage- 
flow. Thus, these snails live much as do many 
species of the sister genus Thcula (Pomati- 
opsidae; Triculinae); this mode of life is not 
that of O. hupensis. 



148 



DAVIS, ZHANG, GUO & SPOLSKY 



NEl'S 1978 D 



DA Lh 


YUNNAN 


S NV 


XI CHANG. 


SICHUAN 


S NV 


JIAN LI. 


HUBEI 


R V 


FU OING. 


FUJIAN 


S V 


XIA PU. 


FUJIAN 


S V 


GUI CHI. 


ANHUI 


R* V 


PENG ZHE, 


JIANGXI 


R* V 



DA LI. 


YUNNAN 


S NV 


XI CHANG. 


SICHUAN 


S NV 


FU QING. 


FUJIAN 


S V 


XIA PU, 


FUJIAN 


S V 


GUI CHI. 


ANHUI 


R« V 


JIAN LI. 


HUBEI 


R V 


PENG ZHE , 


JIANGXI 


П* V 



FIG. 7. UPGMA derived phenograms based on Nei's 1978 D and Arc D for group II populations. 



TABLE 8. Deviations from Hardy-Weinberg (H. W.) equilibrium for all populations studied; P = 
probability; P level accepted = 0.05. 





No. loci 


Locus not 


Probability 






Population 


polymorphic 


in H.W. 


X^ 


pooled 


exact 






GROUP 1 POPULATIONS (29 loci) 






Dali 


4 


SDH-1 


0.01 


— 


0.03 


FuQing 


2 


— 


— 


— 


— 


GuiChi 


6 


EST-3 


0.0 


— 


0.04 


JianLi 


5 


EST-2 


0.01 


0.02 


0.03 






OCT 


0.0 


0.02 


0.03 


PengZhe 


7 


SDH-1 


0.002 


— 


0.01 


XiChang 


1 


— 


— 


— 


— 


XiaPu 


2 


— 


— 


— 


— 






GROUP II POPULATIONS (28 loci) 






ChangXing 


1 


PGM-1 


0.02 


— 


0.03 


TongLing 


4 


EST-2 


0.001 


0.02 


0.04 


JiangLing 


5 


— 


— 


— 


— 


YueYang 


5 


AAT-2 


0.0 


— 


0.02 


GuiPing 


3 


EST-2 


0.0 


— 


0.02 


NingGuo 


5 


EST-2 


0.0 


— 


0.0 


HanYang 


5 


— 


— 


— 


— 



The type of morphological discontinuity 
and ecological divergence that allows recog- 
nition of these two species parallels that of 
the types of character-state changes seen 
among species of the sister subfamily Tricu- 
linae. Closely related triculine species differ 
by a combination of character states, such as 



given above and: penis with papilla in one 
species, without in another; seminal vesicle a 
coil dorsal to the gonad vs. a knot on the 
posterior stomach; penis with pronounced 
ejaculatory duct in the base of the penis in 
one species vs. absent in another; outer mar- 
ginal tooth with specialized outer cusp vs no 



POPULATION GENETICS OF ONCOMELANIA HUPENSIS 



149 



TABLE 9. Matrix of genetic distances (mD) for the combined set of fourteen populations. R = ribbed; S 
= smooth; V = marix; NV = no varix. 



Population 



DA FQ GC 



Jl 



PZ 



XI 



XP ex TL JL YY GP NG HY 



— 0.218 0.209 0.166 0.297 0.110 0.215 0.007 0.101 0.344 0.308 0.296 0.294 0.255 

— 0.266 0.241 0.276 0.225 0.154 0.205 0.254 0.334 0.376 0.453 0.296 0.404 

— 0.202 0.247 0.270 0.262 0.203 0.204 0.299 0.245 0.260 0.325 0.286 

— 0.274 0.232 0.234 0.169 0.156 0.339 0.280 0.378 0.372 0.324 

— 0.275 0.349 0.291 0.208 0.097 0.129 0.231 0.256 0.167 

— 0.266 0.127 0.155 0.292 0.367 0.361 0.328 0.307 

— 0.201 0.243 0.306 0.286 0.357 0.253 0.315 

— 0.092 0.337 0.300 0.290 0.281 0.249 

— 0.262 0.203 0.221 0.217 0.167 

— 0.059 0.199 0.242 0.092 

— 0.150 0.222 0.048 

— 0.232 0.098 

— 0.185 



Dali, Yunnan 


S, NV 


FuQing, Fujian 


S, V 


GuiChi, Anhui 


R+, V 


JianLi, Hubei 


R, V 


PengZe, Jiangxi 


R+, V 


XiChang, Sichuan 


S, NV 


XiaPu, Fujian 


S, V 


ChangXing, Zhejiang 


S, NV 


TongLing, Anhui 


R+, V 


JiangLing, Hubei 


R, V 


YueYang, Hunan 


R+, V 


GuiPing, Guangxi 


S+, V 


NingGuo, Anhui 


S, V 


HanYang, Hubei 


R+, V 



NEI'S MINIMUM DISTANCE 



£ 



DA LI. 


YUNNAN 


S 


NV 


CHANG XING 


ZHEJIANG 


S 


NV 


TONG LING, 


ANHUI 


fí* 


V 


XI CHANG . 


SICHUAN 


S 


NV 


JIAN LI. 


HUBEI 


R 


V 


GUI CHI. 


ANHUI 


R* 


V 


FU QING. 


FUJIAN 


S 


V 


XIA PU. 


FUJIAN 


S 


V 


PENG ZHE, 


JIANGXI 


R* 


V 


JIANG LING. 


HUBEI 


R 


V 


VUE YANG. 


HUNAN 


R* 


V 


HAN YANG. 


HUBEI 


R4 


V 


GUI PING. 


GUANGXI 


S+ 


V 


NING GUO. 


ANHUI 


S 


V 



FIG. 8. UPGMA derived phenogram based on Nei's minimum D (Table 9) for both population groups 
combined. 



specialized outer cusp; and so forth. In sum, 
species in the Pomatiopsinae and the sister 
clade, Triculinae, regularly demonstrate mor- 
phological discontinuities equatable to con- 
siderable relative genetic divergence. Such 
discontinuity is not found within the On- 
comelania hupensis species complex. 

The Oncomelania hupensis Polytypic 
Species Complex 

The data we have thus far for this species 
indicates that overall cohesiveness — mor- 
phological, genetic, and ecological — has not 
been disrupted to the extent that allopatric 
populations in this complex should be ac- 



corded species status. Nevertheless, evolu- 
tion towards species rank has progressed to 
varying degrees in many allopatric popula- 
tions both within and outside China. 

In China, Oncomelania is distributed in 12 
provinces and 347 counties (Kang, 1985). It 
has been argued by Liu et al. (1981) that, 
based on shell differences, there are five sub- 
species in mainland China: O. Iiupensis hu- 
pensis; O. hupensis robertsoni (Bartsch, 
1946); О. hupensis tangi (Bartsch, 1936b); O. 
hupensis fausti (Bartsch, 1925); and O. hu- 
pensis guangxiensis (Liu et al., 1981). On the 
basis of the data presented here, we are in- 
clined to accept three of them. 

Before discussing allozyme results and the 



150 DAVIS, ZHANG, GUO & SPOLSKY 

О. hupensis hupensis 




O. h. tangi 



FuQing 



XiaPu 



O. h. robertsoni 



0.10 

FIG. 9. An unrooted FITCH tree based on Nei's mD for both population groups combined. Line lengths are 
proportional to branch lengths. 



basis for accepting three subspecies, it is im- 
portant to understand the genetic basis for 
shell characters. Historically, the plesiomor- 
phic relevant character states are: small size, 
smooth shell, no varix, colorless apex (Davis, 



1979). Today, differences among populations 
are seen in the increased shell size, sculpture 
(smooth to heavily ribbed), varix or lack of 
same, width/length ratios, and apex color. 
Hybridization and schistosome susceptibility 



POPULATION GENETICS OF ONCOMELANIA HUPENSIS 



151 



TABLE 10. Comparison of Nei's mD (for mD < 0.157), shell morphology, and geographic distance; S = 
smooth shells; R = ribbed shells (see Table 1 caption). Distances in km. 

0.007 Dali, Yunnan x ChangXing, Zhejiang 

0.048 HanYang, Hubei -- YueYang, Hunan 

0.059 JiangLing, Hubei ■ YueYang, Hunan 

0.092 ChangXing, Zhejiang ■ TongLing, Anhui 

0.092 JiangLing, Hubei - HanYang, Hubei 

0.097 PengZe, Jiangxi ■ JiangLing, Hubei 

0.098 GuiPing, Guangxi ■ HanYang, Hubei 

0.101 Dali, Yunnan x TongLing, Anhui 

0.110 Dali, Yunnan x XiChang, Sichuan 

0.127 XiChang, Sichuan x ChangXing, Zhejiang 

0.129 PengZe, Jiangxi > YueYang, Hunan 

0.150 YueYang, Hunan ■ GuiPing, Guangxi 

0.154 XiaPu, Fujian ■ FuQing, Fujian 

0.155 XiChang, Sichuan ■ TongLing, Anhui 

0.156 JianLi, Hubei ■ TongLing, Anhui 

0.204 GuiChi x TongUng/ANHUI 

0.339 JiangLing x JianLi/HUBEl 



S ■ s 


2,052 (most distant) 


R+ -, R+ 


62.5 


R., R+ 


141.1 


S X R+ 


199.0 


R x R+ 


175.0 


R+ y R 


438.3 


S+ X R+ 


899.3 


S X R+ 


1,854 


S X S 


321.4 


S X S 


1,784 


R+ X R+ 


312.0 


R+ X S+ 


660.0 


SxS 


142.3 


S X R+ 


1,567 


R X R+ 


442.0 


R+ X R+ 


44.4 (closest neighbors) 


R X R 


72.1 



TABLE 11. Pairwise comparisons of Nei's (1978) D values in a gradation from 
small to large values along with the provinces involved. From Tables 4 and 7. 



mD 



Populations compared 



Geographic location 



0.089 


TongLing ' ChangXing 


0.102 


HanYang ■ YueYang 


0.140 


HanYang > GuiPing 


0.155 


GuiPing ■ YueYang 


0.176 


XiaPu ■ Dali 


0.193 


HanYang x NingGuo 


0.221 


GuiChi X Dali 


0.255 


JianLi ■ FuQing 


0.261 


GuiPing - JiangLing 


0.287 


GuiChi X FuQing 


0.292 


GuiChi X XiChang 


0.301 


XiChang ■ PengZe 


0.334 


PengZe ■ Dali 


0.346 


XiaPu ■ PengZe 


0.364 


GuiPing - ChangXing 


0.382 


YueYang ' ChangXing 



Anhui — Zhejiang Provinces 
Hubei Province 
Hubei — Guangxi Provinces 
Guangxi — Hubei Provinces 
Fujian — Yunnan Provinces 
Hubei — Anhui Provinces 
Anhui — Yunnan Provinces 
Hubei — Fujian Provinces 
Guangxi — Hubei Provinces 
Anhui — Fujian Provinces 
Anhui — Sichuan Provinces 
Sichuan — Jiangxi Provinces 
Jiangxi — Yunnan Provinces 
Fujian — Jiangxi Provinces 
Guangxi — Zhejiang Provinces 
Hubei — Zhejiang Provinces 



Studies underscore the importance of these 
sculptural aspects (Davis and Ruff, 1973). 
Ribbing is dominant to smooth, involving a 
single gene with multiple alleles. Large size is 
dominant to small as is higher whorl number. 
Hybrid vigor was demonstrated, as F-, snails 
had 7.5 to 8.5 whorls, whereas parental 
snails had 5.0 to 6.5 whorls. Susceptibility is 
dominant to resistance. In addition to shell 
characters, pigmentation is dominant to albi- 
nism. 

Ribbing is restricted to the mainland of 
China and especially to low-land flood plains 
and marshy areas adjacent to the Yangtze 
River or rivers flowing into the Yangtze. At 
higher elevation, above the effects of annual 



flooding, the shells of snails become smooth. 
All snail populations in the highland areas 
west of the three gorges barrier on the 
Yangtze River, in Yunnan and Sichuan, are 
smooth and without a varix. Ribbing seems 
to be selected for relative to dispersal and 
survival during rampaging floods of the 
Yangtze River drainage. 

The varix, the rib-like thickening at the lip 
of the shell is, it seems, the last rib. Yet, there 
are smooth shells that may or may not have a 
varix. All shells with ribs have a varix. Reten- 
tion of the varix in smooth shells seems to be 
the genetic loss of all ribs except the last one. 
It is also probable that the loss of ribbing with 
retention of the varix has occurred indepen- 



152 



DAVIS, ZHANG, GUO & SPOLSKY 



TABLE 12. Comparison of populations based on shell sculpture using Nei's minimum D 

I. Smooth X Smooth Shells 

Dali X Sichuan x Zhejiang [no varix] 

Fujian [strong, wide varix] 

Dali groups x Fujian group 

NingGuo [smooth, varix] x Dali group 

NingGuo x Fujian group 

GuiPing [smooth, varix] x Dali group 

GuiPing X Fujian group 

II. Ribbed X Ribbed Shells 
All ribbed populations (incl. hybrids) 
Ribbed populations (excluding hybrids) 
(includes HY, GP, YY, PZ, JL, NG = Ribbed "Group of 6") 

III. Smooth X Ribbed 
Dali group X All ribbed populations 
Dali group X Group of 6 
Fujian group x All ribbed populations 
Fujian group x Group of 6 
NingGuo X rest of group of 6 
GuiPing X rest of group of 6 

IV. TongLing [ribbed, possible hybrid] v Other Groups 
TongLing x Dali group 
TongLing x Fujian group 
TongLing x Group of 5 
TongLing x NingGuo 

V. GuiChi [ribbed, possible hybrid] x Other Groups 
GuiChi X Dali group 
GuiChi X Fujian group 
GuiChi X Group of 5 
GuiChi X NingGuo 

VI. JiangLi [ribbed, possible hybrid] x Other Groups 
JiangLi X Dali group 
JiangLi X Fujian group 
JiangLi x Group of 5 
JiangLi X NingGuo 



0.081 ± 0.06 


N 


= 3 


0.154 


N 


= 1 


0.230 ± 0.024 


N 


= 6 


0.301 ±0.024 


N 


= 3 


0.274 


N 


= 2 


0.316 ±0.036 


N 


= 3 


0.405 


N 


= 2 


0.204 ± 0.085 


N 


= 21 


0.160 ±0.092 


N 


= 15 


0.257 ± 0.077 


N 


= 21 


0.304 ± 0.056 


N 


= 18 


0.296 ± 0.053 


N 


= 14 


0.334 ± 0.089 


N 


= 12 


0.227 ± 0.036 


N 


= 5 


0.182 ±0.042 


N 


= 5 


0.116 ±0.032 


N 


= 3 


0.249 


N 


= 2 


0.212 ±0.048 


N 


= 5 


0.217 


N 


= 1 


0.227 ± 0.034 


N 


= 3 


0.264 


N 


= 2 


0.267 ± 0.027 


N 


= 5 


0.325 


N 


= 1 


0.189 ±0.033 


N 


= 3 


0.238 


N 


= 2 


0.319 ±0.052 


N 


= 5 


0.378 


N 


= 1 



dently in different geographic regions and at 
different times. Thus, one observes the fol- 
lowing characters and character-states. 
Varix: absent (0), present (1); Varix shape: 
high and pronounced (0), \o\n and wide (1). 

The subspecies we accept and the basis 
for accepting them are given below: 

Oncomelania hupensis hupensis Gredler, 
1881, is strongly ribbed and with a strong 
rib-like varix. Shells are tall, large. This sub- 
species occurs throughout the mid to lower 
Yangtze River basin, especially Hubei, 
Hunan, and Anhui provinces, and the Bei 
River in Guangdong Province (Liu et a!., 
1981). At first glance, our populations 3, 4, 5, 
9, 10, 11, 12 (Table 1) appear to fit this de- 
scription. Nei's mD among these seven pop- 
ulations is 0.204 ± 0.085 (N = 21). As dis- 



cussed below, however, we also include two 
smooth-shelled populations, 8 and 13, within 
this grouping, but exclude ribbed popula- 
tions 3, 5, and 12. 

We included within O. hupensis hupensis 
the nominal subspecies O. h. fausti and O. h. 
guangxiensis. Onconnelania h. fausti has O. h. 
hupensis-s\zed shells that are smooth but 
with a strong varix. These smooth-shelled 
snails live in uplands beyond the reach of 
flooding of the Yangtze River and tributaries. 
The two nominal taxa live over the same geo- 
graphical regions. Lou et al. (1982) con- 
cluded that they are synonymous. In Hubei 
Province, one finds streams where the 
smooth form is at the headwaters and the 
ribbed form is along the flood plain. In inter- 
mediate zones, there appears to be intergra- 



POPULATION GENETICS OF ONCOMELANIA HUPENSIS 



153 



dation of the two sculptural types. It is ap- 
parent that ribbing is associated with flood 
plains and the smooth shells associated with 
upland areas beyond the effects of flooding. 
There are no physical or reproductive barriers 
between the sculptural types. The upland 
habitats only reflect elevation and freedom 
from annual flooding, not differences in the 
microhabitat. The one population of the 
"fausti" type that we studied, no. 13 from 
Ning Quo, Anhui Province, differs from the 
other members of the coherent group of six 
ribbed populations (Table 12) by an mD of 
0.227 ± 0.062 (N = 13); from the two smooth- 
shelled groups, Dali and Fujian, by 0.301 and 
0.274, respectively. Further, in both phyloge- 
netic analyses (Figs. 8, 9), this "fausti" type 
clusters with the group of predominantly 
ribbed-shelled taxa. We noted previously 
that Nei's mD for the latter populations is 
0.160 ± 0.07. Accordingly, we do not con- 
sider O. h. fausti to be a distinct subspecies 
but a smooth form of O. h. hupensis. 

Liu et a!. (1981) described a new subspe- 
cies, O. hupensis guangxiensis from the 
northwestern part of Guangxi along the Yu 
Jiang and Hongshui river systems. The shells 
were described as medium sized, rather thin, 
smooth and with a weak varix. The type and 
the description of the taxon puts emphasis 
on deep sutures and especially rounded 
body whorl. Our Guangxi population from Gui 
Ping is at the confluence of the Yu Jiang and 
Hongshui rivers. One of our specimens re- 
sembles the figured type, but the remaining 
somewhat resemble the "O. Ii. fausti" type. 
The shells are smooth and the varix weak in 
90% of the snails. However, there are weak 
scattered ribs or pronounced growth lines on 
the shells of some individuals. It differs from 
the two smooth-shelled groups by Nei's mD 
of 0.316 and 0.405 respectively; it differs 
from the other members of the coherent 
group of six ribbed populations by 0.182. As 
■with our "fausti" population, this population 
clusters even more tightly with the coherent 
group of O. A), fiupensis. The faint ribs seen 
on some shells and its genetic affinity for taxa 
in the lower cluster indicates to us that it is 
part of the ribbed-shell group, i.e. O. /?. fiu- 
pensis, and not a distinct subspecies. How- 
ever, topotypes must be studied to confirm 
our opinion. 

This then brings into question the affinity of 
the three ribbed populations in the upper 
cluster of Figure 8, Tong Ling, Jian Li, and 
Gui Chi. Because morphologically and geo- 



graphically, these populations appear to be 
O. h. tiupensis, but genetically and phyloge- 
netically, they appear most closely allied to 
the smooth-shelled Dali group, we raise the 
possibility that these three populations are a 
result of hybridization between smooth- 
shelled taxa, such as O. h. robertsoni as dis- 
cussed below (Dali, Chang Xing, and Xi 
Chang), and a ribbed O. h. fiupensis popula- 
tion. It is particularly compelling to make this 
hypothesis given: (1) that ribbing is dominant 
to smooth and the populations in question 
come from the flood plains; (2) an average 
mD to the three O. h. robertsoni populations 
of only 0.116 ± 0.034; and (3) the close geo- 
graphic proximity of the Tong Ling population 
and the transported smooth-shelled popula- 
tion from Chang Xing, Zhejiang Province; the 
genetic distance between these two popula- 
tions is only 0.092. In further discussion, 
when we refer to ribbed populations, we 
therefore include only the coherent group of 
six populations that cluster together in phy- 
logenetic analyses (Figs. 8, 9). 

Oncomelania fiupensis robertsoni (our 
populations Dali, Xi Chang, Chang Xing) is 
smooth and without varix. It is located in Si- 
chuan and Yunnan provinces at altitudes 
from 200 m up to 2,000 m (Liu et al., 1981) in 
ditches along the slopes of hills, at the edges 
of fields and irrigation canals in basin areas. 
The geographic region is isolated from other 
provinces with respect to invasion down the 
Yangtze River by the long stretch of the 
treacherous Yangtze Gorges west of Hubei 
Province. One population assigned to this 
subspecies is enigmatic in that it comes from 
Zhejiang Province at the eastern end of China 
(Group II, Chang Xing), a locality that is the 
farthest removed from Yunnan-Sichuan of all 
populations studied, yet the least divergent 
ifrom the Yunnan population (Nei's mD of 
0.007). The presence of this population can- 
not be due to dispersal by flotation down the 
Yangtze, given the time involved to disperse 
over such a great distance and the genetic 
near-identity, but rather to a recent introduc- 
tion either by man or birds. These three pop- 
ulations cluster together tightly by both 
methods of analysis (Figs. 8, 9; mD = 0.081). 
They differ from the ribbed group (O. h. fiu- 
pensis) by an average mD of 0.305 ± 0.071 (N 
= 34). They also differ from the smooth- 
shelled Fujian group (O. hupensis tangí) by 
0.220 ± 0.024. Thus, there is a significant dif- 
ference in genetic distance between these 
two smooth-shelled groups. 



154 



DAVIS, ZHANG, GUO & SPOLSKY 



Oncomelania hupensis tangí (our Fu Qing, 
Xia Pu populations) has smooth shells with a 
low but very wide varix. The width of the 
shells is greater relative to height than in O. h. 
robertsoni. Oncomelania h. tangi lives along 
the coast of Fujian Province in hilly environ- 
ments (from 50 to 500 m altitude) as well as in 
small ditches of the seaside lowlands. This 
region is very isolated from other regions with 
Oncomelania (Fig. 1). Our two populations 
form a separate cluster (Figs. 8, 9); they differ 
from all others by an mD of 0.285 ± 0.066 (N 
= 24); from the ribbed group by 0.334 ± 0.089 
(N = 10). Given an intragroup mD of 0.154, 
there is a decided gap between this taxon 
and O. h. hupensis or O. h. robertsoni. 

There are no fixed diagnostic alleles unique 
to any of the nominal subspecies. While ge- 
netic distance per se is not a measure of sub- 
species status, a subspecies should be co- 
herent genetically as well as morphologically. 
Phylogenetic clusters shown in Figs. 8 and 9 
do provide evidence for genetic cohesive- 
ness supporting the three subspecies we ac- 
cept, if the arguments we provided concern- 
ing "fausti," "guangxiensis," and possible 
hybhds hold up. Additional arguments to 
support the subspecies are: (1) regional iso- 
lation; (2) shell size/shape; (3) presence or 
absence of shell ribbing, but recognizing that 
hybridization in the flood plains will yield a 
ribbed shell; (4) presence or absence of 
varix; (5) varix, if present, low and wide (0), 
weak (1), strong and rib-like (2); (6) differ- 
ences in susceptibility to schistosomes (Liu 
et al., 1981); (7) low interpopulation genetic 
distances as well as low percentage of poly- 
morphic loci within the O. h. robertsoni and 
O. h. tangi smooth-shelled groups, as well as 
within the coherent O. h. hupensis group. 

Hope and McManus (1994) carried out 
PCR-based RFLP analyses of variation in the 
ITS-region of rDNA repeat unit among four 
populations of Oncomelania hupensis in 
China, three from the Philippines, and one 
from Japan. Their data are puzzling because 
the largest divergence they find is between 
the Yunnan and Sichuan populations in 
China, populations we classify as O. hupen- 
sis robertsoni because of cohesiveness in al- 
lozymes, shell sculpture, lack of varix, and 
biogeographic closeness; and additionally, 
because of lowest divergences among pop- 
ulations in cytochrome b gene sequences 
(Spolsky and Davis, unpubl.). The discrep- 
ancy may be the result of the paucity of data 
points (DNA fragment bands) in the RFLP 



analyses and of the inability to distinguish 
small differences in fragment size. We there- 
fore advise caution in choice of tool to dem- 
onstrate population divergence. All studies of 
populations should give illustrations of the 
shells to ascertain shell phenotypes. Voucher 
specimens should be deposited for refer- 
ence. 



SUMMARY 

The assortment of four shell characters to 
distinct geographic regions and regional in- 
fectivity patterns argue for subspecific sta- 
tus. Low allozymic heterozygosity, unique 
combinations of shell characters, coherent 
genetic clustering and geographic isolation 
indicate the usefulness of recognizing sub- 
species for two smooth-shelled taxa. The 
presence of a different type of varix on the 
shells of these two nominal subspecies indi- 
cates to us that they had independent ori- 
gins. The phylogenetic analyses confirm this. 

Major points to be considered are: 

1 . The three regional sets of populations 
should be treated as subspecies. Allozyme 
differences are insufficient by themselves, 
but together with geographic location and 
shell characters, enable recognition of each 
of these population sets as subspecies. 

2. In hilly areas above the Yangtze River 
flood effects, ribbing becomes reduced and 
lost. This does not affect subspecific status. 

3. The disjunction between morphology 
and genetic distance in three ribbed popula- 
tions indicates possible hybridization be- 
tween subspecies, in particular between O. 
h. robertsoni and O. h. hupensis. 

4. The considerable interpopulation ge- 
netic distance between allopatric popula- 
tions of the same shell type, especially in the 
O. hupensis hupensis complex (that includes 
all populations with ribs), shows genetic 
change in the absence of anatomical change. 
We predict that there would be parallel ge- 
netic differences in the populations of Schis- 
tosoma japonicum transmitted by these allo- 
patric snail populations: such genetic 
differentiation should be visible in DNA se- 
quences of genes such as cytochrome b. 
Molecular differences in the snails and their 
parasites evolve at a different tempo and 
mode than does the anatomical ground plan. 
Would sufficient differences be found to de- 
fine a series of morphostatic (term defined in 
Davis, 1992) subspecies where differences 



POPULATION GENETICS OF ONCOMELANIA HUPENSIS 



155 



might be driven by localized parasitism in a 
tightly coevolved system as suggested by 
Davis (1992)? 

5. A weakness of this paper is that there was 
not enough material to confirm the allele align- 
ments on which the integrated data set in 
Table 9 is based. Each data set by itself is 
confirmed. What is now needed are: (1) a de- 
tailed analysis of populations within a prov- 
ince grouped along river drainage systems 
from highlands to point of entry to the Yangtze 
River or other primary river; (2) a comparison 
between selected populations of the different 
subspecies using more than 50 snails per 
population in order to increase reliability in 
estimates of polymorphic loci; (3) a careful 
analysis of populations of O. hupensis hupen- 
sis from selected streams where there is a 
demonstrated change from ribbed shells on 
the flood plains to smooth shells at higher 
elevations. 

Clearly, this baseline study has set the 
stage for future, carefully targeted studies. 



ACKNOWLEDGMENTS 

We thank Caryl Hesterman for running the 
gels; all gels were scored by Davis. Graphics 
were prepared by Susan Trammell. We are 
indebted to Dr. Margaret Mulvey and to Dr. 
Hsiu-Ping Liu of the Savannah River Ecology 
Laboratory for their independent critical re- 
view of the manuscript; they made valuable 
suggestions for improvement. This work was 
supported by N.I.H. grant TMP AI 11373 to 
Davis. The support of the Institute of Parasitic 
Diseases, Chinese Academy of Preventive 
Medicine is gratefully acknowledged. 



LITERATURE CITED 

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AYALA, F. & С F. AQUADRO, 1982, A comparative 
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Evolutionary Biology, 15: 151-158. 

AYALA, F., D. HEDGECOCK, G. ZUMWALT & J. 
VALENTINE, 1973, Genetic variation in Tridacna 
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177-191. 

BARTSCH, P., 1925, Some new intermediate hosts 
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BARTSCH, P., 1936a, Molluscan intermediate 
hosts of the Asiatic blood fluke. Schistosoma 
japonicum, and species confused with them. 
Smithsonian Miscellaneous Collections, 95: 
1-60, 8 pis. 

BARTSCH, P., 1936b, A new intermediate host of 
the Asiatic blood fluke. Schistosoma japonicum. 
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BARTSCH, P., 1946, Schistosomophora in China, 
with descriptions of two new species and a note 
on their Philippine relative. Smithsonian Miscel- 
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CAVALLI-SFORZA, L. L. & A. W. EDWARDS, 1967, 
Phylogenetic analysis: models and estimation 
procedures. Evolution, 21: 550-570. 

DAVIS, G. M., 1971, Mass cultivation of Oncomel- 
ania (Prosobranchia: Hydrobiidae) for studies of 
Schistosoma japonicum. Bio-Medical Reports of 
the 406th Medical Laboratory, 19: 85-161. 

DAVIS, G. M., 1 979, The origin and evolution of the 
gastropod family Pomatiopsidae, with emphasis 
on the Mekong River Triculinae. Monograph of 
the Academy of Natural Sciences of Philadel- 
phia, 20: 1-120. 

DAVIS, G. M., 1980, Snail hosts of Asian Schisto- 
soma infecting man: origin and coevolution. In: j. 
BRUCE ET AL., eds. The Mekong schistosome. Ma- 
lacological Reviev\/, Supplement, 2: 195-238. 

DAVIS, G. M., 1981, Different modes of evolution 
and adaptive radiation in the Pomatiopsidae 
(Prosobranchia: Mesogastropoda). Malacologia, 
21: 209-262. 

DAVIS, G. M., 1983, Relative roles of molecular 
genetics, anatomy, morphometries, and ecology 
in assessing relationships among North Ameri- 
can Unionidae (Bivalvia). In: g s oxford & d. roll- 
iNsoN, eds. Protein polymorphism: adaptive and 
taxonomic significance. Systematics Association 
Special Volume, 24: 193-221. Academic Press. 

DAVIS, G. M., 1992, Evolution of prosobranch 
snails transmitting Asian Schistosoma; coevolu- 
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Clinical Parasitology 3: 145-204. 

DAVIS, G. M., 1994, Molecular genetics and taxo- 
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2: 3-23. 

DAVIS, G. M., W. H. HEARD, S. L H. FULLER, & С 
HESTERMAN, 1981, Molecular genetics and 
speciation in Elliptic and its relationships to other 
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DAVIS, G. M., С E. CHEN, Z. B. KANG & Y. Y. LIU, 
1994a, Snail hosts of Paragonimus in Asia and 
the Americas. Biomedical and Environmental 
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DAVIS, G. M., С E. CHEN, X. P. ZENG, S. H. YU & 
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DAVIS, ZHANG, GUO & SPOLSKY 



DAVIS, G. M., V. FORBES & G. LOPEZ, 1 988, Spe- 
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DAVIS, G. M., M. MCKEE & G. LOPEZ, 1989, 
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359. 

DAVIS, G. M. & M. RUFF, 1973, Oncomelania hu- 
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DILLON, R. & G. M. DAVIS, 1980, The Goniobasis 
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FELSENSTEIN, J., 1989, PHYLIP— Phylogeny In- 
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HAASE, M., 1993, The genetic differentiation in 
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HOPE, M. & D. P. McMANUS, 1994, Genetic vari- 
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JOHNSON, M. S., O. С STINE & J. MURRAY, 
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KANG, Z. В., 1981, A review of the taxonomical 
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KANG, Z. В., 1985, Comments on some problems 
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LIU, Y. Y., T. K. LOU, Y. X. WANG & W. Z. ZHANG, 
1981, Subspecific differentiation of oncomela- 



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LOU, T. Z., Y. Y. LIU, W. Z. ZHANG & Y. X. WANG, 
1982, A discussion on the classification of On- 
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pis. 

MURRAY, J., O. С STINE & M. S. JOHNSON, 
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Partula. Heredity, 66: 93-104. 

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PATTERSON, H. E. H., 1985, The recognition con- 
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speciation. Transvaal Museum Monograph, 4: 
21-29. Pretoria, South Africa. 

RICE, W. R., 1989, Analyzing tables of statistical 
tests. Evolution, 43: 223-225. 

ROSENBERG, G., 1989, Phylogeny and evolution 
of terrestriality of the Atlantic Truncatellidae 
(Prosobranchia: Gastropoda: Mollusca). Unpubl. 
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STINE, O. C, 1989, Cepaea nemoralis from Lex- 
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SWOFFORD, D. L. & R. SE1J\NDER, 1981, BIO- 
SYS-1. A computer program for the analysis of 
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TEMPLETON, A. R., 1 989, The meaning of species 
and speciation: a genetic perspective. In: d. otte 
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Sunderland, Mass. 

VAN DER SCHALE, H. & G. M. DAVIS, 1968, Cul- 
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drobiidae) for studies of oriental schistosomia- 
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WOODRUFF, D., К. С. STAUB, E. S. UPATHAM, V. 
VIYANT & H. С. YUAN, 1 988, Genetic variation in 
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transmitting snails in China and the Philippines 
are distinct species. Malacologia, 29: 347-361. 

Revised Ms. accepted 1 June 1995 



MAU\COLOGIA, 1995, 37(1): 157 



LETTER TO THE EDITOR 



RESPONSE TO BOUCHET & ROCROI; "THE LOTTERY OF BIBLIOGRAPHICAL 
DATABASES: A REPLY TO EDWARDS & THORNE" 

M. A. Edwards^ & M. J. Thorne^ 



While not wishing to protract this exchange 
unnecessarily, we would like to offer a final, 
brief, response to the above. 

Which Names Get Omitted? 

The analysis of names omitted is based on 
material published mostly between 1940 and 
1975, that is between 20 and 55 years ago. 
During most of this period the Record was 
compiled by volunteer specialists in the dif- 
ferent animal groups. The work was done in 
their spare time so that, while it is unfortu- 
nate, it is not surprising that material, whether 
from obscure or main stream publications, 
was overlooked. 

Bouchet & Rocroi say that ". . . in an era of 
frequent and easy travel . . . the staff of ZR 
has attended only once ... an International 
Malacological Congress . . ." and, atten- 
dance at meetings would ". . . greatly en- 
hance the efficiency of Zfî . . .". 

There is a simple explanation for our ab- 
sence at meetings and that is although travel 
may be easy, it is expensive. We are occa- 
sionally able to attend local meetings (hence 
our presence at the 1986 congress in Edin- 
burgh), but the cost of attending the annual 
and other meetings of all the main zoological 
disciplines in Europe, USA, Russia, or any- 
where else, is quite beyond the capacity of 
our budget. As referred to in our earlier re- 
sponse, Zoological Record production is 



heavily subsidized, and increased travel 
would add considerably to the already large 
overheads borne by BIOSIS. 

It must also be said that while the meetings 
we have attended have certainly been useful, 
they have not led to the discovery of signifi- 
cant numbers of new titles for indexing. 

The Risks of a "List of Available Generic 
Names in Zoology" Based on Nomenclátor 
Zoologicus and ZR" 

The policy of the Zoological Record and 
the Nomenclátor Zoologicus is to provide in- 
formation and not to adjudicate on the status 
of the names listed. The Nomenclátor seeks 
to give details of the first use of a name and 
it is not practical to check back on previous 
volumes to determine the availability of 
names under the Code. A note of any rele- 
vant information on errors, omissions, and 
other matters is always welcomed by the ed- 
itor for future action. 

As mentioned above. The Zoological 
Record is subsidized by BIOSIS and the No- 
menclátor Zoologicus is compiled on a vol- 
untary basis. Each is produced as a service 
to zoology and not as a financial proposition. 

It is our understanding that proposals on 
how a registry of names might be compiled 
or made available have yet to be finalized, 
therefore further discussion seems prema- 
ture. 

The editor-in-chief of Malacologie welcomes let- 
ters that comment on vital issues of general im- 
portance to the field of Malacology, or that com- 
ment on the content of the journal. Publication is 
dependent on discretion, space available and, in 
some cases, review. Address letters to: Letter to 
the Editor, Malacologia, care of the Department 
of Malacology, Academy of Natural Sciences, 
19th and the Parkway, Philadelphia, PA 19103. 



^The Zoological Society of London, Regent's Park, London, NWI 4RY, United Kingdom. 
^BIOSIS, U.K., Garforth House, 54 Micklegate, York, North Yorkshire Y01 1LF, United Kingdom. 



157 



ERRATA 



Ibanez, M., E. Ponte-Lira & M. R. Alonso. 1995. EL GENERO 
CANARIELLA HESSE, 1918, Y SU POSICIÓN EN LA FAMILIA 
HYGROMIIDAE (GASTROPODA, PULMONATA, HELICOIDEA). 
MALACOLOGIA 36(1-2): 111-137. 

Figures 12-20 are reprinted here that include the scale bar under 
Figs. 1 9 and 20. The scale bar, and the edges of the shells at the 
bottoms of figures 1 5 and 1 6 were cut out in the original printing. 



158 




FIGS. 12-20. Concha y SEM detalles. (12) Canariella discobolus (Barranco de la Rajita, La Gomera). (13) 
Canariella gomerae. Lectotipo de Helix (Gonostoma) gomerae (NHM; es un ejemplar pequeño dentro de la 
especie). (14-15) Canariella iiispidula. (14) Lectotipo de Helix (Gonostoma) hispidula subhispidula (ZMZ). 
(15) Lectotipo de Helix (Ciliella) lanosa (ZMZ). (16) Canariella leprosa (El Draguillo, Tenerife). (17-18) Cana- 
riella eutropis. (17) Lectotipo de Helix eutropis (NMB). (18) Mandíbula de un ejemplar de Morro del Cava- 
dero, Fuerteventura). (19-20) Rádula de Canariella planaria (Benijo, Tenerife). (19) Diente central y primeros 
dientes laterales. (20) Dientes laterales próximos al margen radular. Escala: (12-17) 5 mm; (18) 200 |дт; 
(19-20) 20 цт. 



Publication dates 

Vol. 28, No. 1-2 19 Jan. 1988 

Vol. 29, No. 1 28 June 1988 

Vol. 29, No. 2 16 Dec. 1988 

Vol. 30, No. 1-2 1 Aug. 1989 

Vol. 31, No. 1 29 Dec. 1989 

Vol. 31, No. 2 28 May 1990 

Vol. 32, No. 1 30 Nov. 1990 

Vol. 32, No. 2 7 June 1991 

Vol. 33, No. 1-2 6 Sep. 1991 

Vol. 34, No. 1-2 9 Sep. 1992 

Vol. 35, No. 1 14 July 1993 

Vol. 35, No. 2 2 Dec. 1993 

Vol. 36, No. 1-2 8 Jan. 1995 



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VOL. 37, NO. 1 MALACOLOGIA 1995 

CONTENTS 

M. LAZARIDOU-DIMITRIADOU 

The Life Cycle, Demographic Analysis, Growth and Secondary Production of the 
Snail Helicella (Xerothracia) Pappi (Schutt, 1962) (Gastropoda Pulmonata) in E. 
Macedonia (Greece) 1 

HILARY PIGGOTT & GEORGES DUSSART 

Egg-Laying and Associated Behavioural Responses of Lymnaea Peregra 
(Müller) and Lymnaea Stagnalis (L.) to Calcium in their Environment 13 

LUIZ RICARDO LOPES DE SIMONE 

Anatomical Study on Tonna Galea (Linné, 1 758) and Tonna Maculosa (Dillwyn, 

1817) (Mesogastropoda, Tonnoidea, Tonnidae) from Brazilian Region 23 

J. D. ACUÑA & M. A. MUÑOZ '^ ' ~ ' У' 

A Taxonomic Application of Multivariate Mixture Analysis in Patellidae 33 

N. ELEUTHERIADIS & M. LAZARIDOU-DIMITRIADOU 

The Life Cycle, Population Dynamics, Growth and Secondary Production of the 
Snail Viviparus Contectus (Millet) (Gastropoda: Prosobranchia) in the Marshes of 
the River Strymonas, Serres, Macedonia, Northern Greece 41 

KATERINE COSTIL & JACOUES DAGUZAN 

Comparative Life Cycle and Growth of two Freshwater Gastropod Species, 
Planorbarius Corneas (L.) and Planorbis Planorbis (L.) 53 

KENNETH С EMBERTON 

When Shells Do Not Tell: 145 Million Years of Evolution in North America's 
Polygyhd Land Snails, with a Revision and Conservation Priorities 69 

A. HONÉK 

Geographic. Distribution and Shell Colour and Banding Polymorphism in Mar- 
ginal Populations of Cepaea Nemoralis (Gastropoda, Helicidae) 111 

R. VITTURI, A. LIBERTINI, M. PANOZZO & G. MEZZAPELLE 

Karyotype Analysis and Genome Size in Three Mediterranean Species of Peri- 
winkles (Prosobranchia: Mesogastropoda) » 1 23 

GEORGE M. DAVIS, ZHANG Yl, GUO YUAN HUA & CHRISTINA SPOLSKY 

Population Genetics and Systematic Status of Oncomelania Hupensis (Gas- 
tropoda: Pomatiopsidae) Throughout China 133 

LETTER TO THE EDITOR 

M. A. EDWARDS & M. J. THORNE 

Response to Bouchet & Rocroi; "The Lottery of Bibliographical Databases: Л 

A Reply to Edwards & Thorne" 1 57 'Щ 



. [^ 1996 



Ь\ 



MALACOLOGIA 



nternational Journal of Malacology 
Revista Internacional de Malacologia 
Journal International de Malacologie 
Международный Журнал Малакологии 
Internationale Malakologische Zeitschrift 



MALACOLOGIA 

Editor-in-Chief: 
GEORGE M. DAVIS 

Editorial and Subscription Offices: 

Department of Malacology 

The Academy of Natural Sciences of Philadelphia 

1900 Benjamin Franklin Parkway 

Philadelphia, Pennsylvania 19103-1195, U.S.A. 



EUGENE COAN 

California Academy of Sciences 

San Francisco, CA 



Co-Editors: 



Assistant Managing Editor: 

CARYL HESTERMAN 

Associate Editors: 



CAROL JONES 
Denver, CO 



JOHN B. BURCH 
University of Michigan 
Ann Arbor 



ANNE GISMANN 
Maadi 

Egypt 



MAIJ\COLOGIA is published by the INSTITUTE OF MALACOLOGY, the Sponsor Members of 
which (also serving as editors) are: 



RÜDIGER BIELER 
Field Museum, Chicago 

JOHN BURCH 

MELBOURNE R. CARRIKER, 

President Elect 

University of Delaware, Lewes 

GEORGE M. DAVIS 
Secretary and Treasurer 

CAROLE S. HICKMAN, President 
University of California, Berkeley 



AU\N KOHN 

University of Washington, Seattle 

JAMES NYBAKKEN 

Moss Landing Marine Laboratory 

California 

CLYDE F. E. ROPER 
Smithsonian Institution 
Washington, D.C. 

SHI-KUEI WU 

University of Colorado Museum, Boulder 



Participating Members 

EDMUND GITTENBERGER JACKIE L. VAN GOETHEM 

Secretary, iJNITAS MALACOLOGICA Treasurer, UNITAS MALACOLOGICA 

Rijksmuseum van Natuurlijke Koninklijk Belgisch Instituut 

Historie voor Natuurwetenschappen 

Leiden, Netherlands Brüssel, Belgium 



J. FRANCIS ALLEN, Emérita 
Environmental Protection Agency 
Washington, D.C. 

KENNETH J. BOSS 

Museum of Comparative Zoology 

Cambridge, Massachusetts 



Emeritus Members 

ROBERT ROBERTSON 

The Academy of Natural Sciences 

Philadelphia, Pennsylvania 

W. D. RUSSELL-HUNTER 
Easton, Maryland 



Copyright © 1 996 by the Institute of Malacology 



1996 
EDITORIAL BOARD 



J. A. ALLEN 

Marine Biological Station 

Millport, United Kingdom 

E. E. BINDER 

Muséum d'Histoire Naturelle 
Genève, Switzerland 

A. J. CAIN 

University of Liverpool 

United Kingdom 

P. CALOW 

University of Sfieffield 
United Kingdom 

J. G. CARTER 

University of North Carolina 

Chapel Hill, U.S.A. 

R. COWIE 
Bishop Museum 
Honolulu, HI., U.S.A. 

A. H. CLARKE, Jr. 
Portland, Texas, U.S.A. 

B. С CLARKE 
University of Nottingham 
United Kingdom 

R. DILLON 

College of Charleston 

SC, U.S.A. 

C. J. DUNCAN 
University of Liverpool 
United Kingdom 

D. J. EERNISSE 
California State University 
Fu nerton, U.S.A. 

E. GITTENBERGER 

Rijksmuseum van Natuurlijke Historie 
Leiden, Netherlands 



F. GIUSTI 
Université di Siena, 



Italy 



A. N. GOLIKOV 
Zoological Institute 
St. Petersburg, Russia 



S. J. GOULD 
Harvard University 
Cambridge, Mass., U.S.A. 

A. V. GROSSU 
Universitatea Bucuresti 
Romania 

T HABE 
Tokai University 
Shimizu, Japan 

R. HANLON 

Marine Biomedical Institute 

Galveston, Texas, U.S.A. 

J. A. HENDRICKSON, Jr. 
Academy of Natural Sciences 
Philadelphia, PA, U.S.A. 

D. M. HILLIS 
University of Texas 
Austin, U.S.A. 

K. E. HOAGLAND 

Association of Systematics Collections 

Washington, DC, U.S.A. 

B. HUBENDICK 

Naturhistoriska Museet 
Göteborg, Sw/eden 

S. HUNT 
Lancashire 
United Kingdom 

R. JANSSEN 

Forschungsinstitut Senckenberg, 
Frankfurt am Main, Germany 

R. N. KILBURN 

Natal Museum 
Pietermaritzburg, South Africa 

M. A. KLAPPENBACH 

Museo Nacional de Historia Natural 

Montevideo, Uruguay 

J. KNUDSEN 

Zoologisk Institut & Museum 

Kobenhavn, Denmark 

A. LUCAS 

Faculté des Sciences 

Brest, France 

С MEIER-BROOK 
Tropenmedizinisches Institut 
Tübingen, Germany 



H. к. MIENIS 

Hebrew University of Jerusalem 

Israel 

J. E. MORTON 
The University 
Auckland, New Zealand 



A. STANCZYKOWSKA 
Siedlce, Poland 

F. STARMÜHLNER 

Zoologisches Institut der Universität 

Wien, Austria 



J. J. MURRAY, Jr. 
University of Virginia 
Charlottesville, U.S.A. 



Y. I. STAROBOGATOV 
Zoological Institute 
St. Petersburg, Russia 



R. N ATAR A J AN 

Marine Biological Station 

Porto Novo, India 

J. 0KLAND 
University of Oslo 
Norway 

J. OKUTANI 
University of Fisheries 
Tokyo, Japan 

W. L PARAENSE 

Instituto Oswalde Cruz, Rio de Janeiro 

Brazil 

J. J. PARODIZ 
Carnegie Museum 
Pittsburgh, U.S.A. 

J. P. POINTER 

Ecole Pratique des Hautes Etudes 

Perpignan Cedex, France 

W. F. PONDER 
Australian Museum 
Sydney 

Ol Z. Y. 

Academia Sinica 

Qingdao, People's Republic of China 



W. STREIFF 
Université de Caen 
France 

J. STUARDO 
Universidad de Chile 
Valparaiso 

S. TILLIER 

Muséum National d'Histoire Naturelle 

Pans, France 

R. D. TURNER 
Harvard University 
Cambridge, Mass., U.S.A. 

J.A.M. VAN DEN BIGGELAAR 
University of Utrecht 
The Netherlands 

J. A. VAN EEDEN 
Potchefstroom University 
South Africa 

N. H. VERDONK 
Rijksuniversiteit 
Utrecht, Netherlands 



D. G. REID 

The Natural History Museum 

London, United Kingdom 

N. W. RUNHAM 

University College of North Wales 

Bangor, United Kingdom 



B. R. WILSON 

Dept. Conservation and Land Management 

Kallaroo, Western Australia 

H. ZEISSLER 
Leipzig, Germany 



S. G. SEGERSTRLE 
Institute of Marine Research 
Helsinki, Finland 



A. ZILCH 

Forschungsinstitut Senckenberg 

Frankfurt am Main, Germany 



MAIJ\COLOGIA, 1996, 37(2): 163-332 

ANATOMY AND SYSTEMATICS OF THE WESTERN ATLANTIC ELLOBIIDAE 
(GASTROPODA: PULMONATA) 

Antonio M. de Prias Martins 

Departamento de Biología, Universidade dos Acores, P-9502 Ponta Delgada Codex, 

Sao Miguel, Acores, Portugal 

ABSTRACT 

Various conchological, radular and anatomical characters of the 18 Western Atlantic species 
of the pulmonate family Ellobiidae are evaluated and used in a systematic review of the family. 
The conchological features, especially protoconch, resorption of inner whorls, apertural den- 
tition and radular morphology, are useful at the specific and generic levels. Features of the 
radula of the Melampinae change greatly with increasing age. The youngest individuals have 
strongly cusped crowns. Although the cusps usually disappear with age, some species retain 
various features of the juvenile radula. The reproductive and central nervous systems are most 
useful in defining subfamilial relationships. The monaulic, entirely glandular condition of the 
palliai gonoducts, and the greater width of the visceral nerve ring are hereby considered 
primitive. Morton's (1955c) subfamilial division of the halophilic Ellobiidae is corroborated. The 
Pythiinae have a monaulic, entirely glandular palliai gonoduct and a wide visceral nerve ring. 
The Ellobiinae have a diaulic reproductive system with entirely glandular palliai gonoducts, and 
a long visceral nerve ring. The Pedipedinae have a monaulic/incipient semidiaulic, partly glan- 
dular palliai gonoduct, and a concentrated visceral nerve ring. The Melampinae are character- 
ized by an advanced semidiaulic reproductive system with nonglandular palliai gonoducts, and 
concentration of the ganglia of the visceral nerve ring. 

The present work documents that Microtralia Dall, 1894, belongs in the Pedipedinae, not in 
the Melampinae; that Laemodonta Philippi, 1846, belongs in the Pythiinae, not in the Pedipe- 
dinae; that Leuconia succinea Pfeiffer, 1854, belongs in the Pedipedinae and in the new genus 
Creedonia; that Apodosis Pilsbry & McGinty, 1949, is synonymous with Leuconopsis Hutton, 
1 884; that Myosotelia Monterosato, 1 906, type species Myosotella payraudeaui "Shuttleworth" 
Pfeiffer, 1856 [= Auricula myosotis Draparnaud, 1801], is removed from Ovatella Bivona, 1832, 
and restored to generic rank; that Detracia Gray, 1840, as noted by Zilch (1959), is a subgenus 
o^ Melampus Montfort, 1810; that Melampus monile (Bruguière, 1789) belongs in the subgenus 
Detracia Gray, 1840; and that Detracia clarki Morrison, 1951, is a junior secondary homonym 
and is herein renamed Melampus (Detracia) morhsoni. Leuconopsis manningi new species, 
from Ascension Island, is described. 

The phylogenetic relationships within the Ellobiidae are discussed, a tentative cladogram of 
the family is presented, some distributional patterns are considered and reference is made to 
the fossil record. 

Key words: Archaeopulmonata, Ellobiidae, systematics, shell, radula, anatomy, genitalia, 
nervous system. Western Atlantic, mangroves, salt marshes. 



TABLE OF CONTENTS 

Introduction Ellobium (Auriculodes) dominicense 

Materials and Methods (Férussac, 1821) 

Abbreviations Used in Figures Genus Blauneria Shuttleworth, 1854 

Taxonomic Characters Blauneria heteroclita (Montagu, 1808) 

Classification Outline, Western Atlantic Ellobiidae Subfamily Pythiinae Odhner, 1925 

Systematics Genus Myosotella Monterosato, 1906 

Family Ellobiidae H. & A. Adams in Pfeiffer, Myosotella myosotis (Draparnaud, 1801) 

1854 Genus Laemodonfa Philippi, 1846 

Subfamily Ellobiinae H. & A. Adams in Pfeiffer, Laemodonta cubensis (Pfeiffer, 1854) 

1854 Subfamily Pedipedinae Fischer & Crosse, 1880 

Genus Ellobium Roding, 1798 Genus Pedipes Scopoli, 1777 

Subgenus Auriculodes Strand, 1928 Pedipes mirabilis (Mühlfeld, 1816) 

163 



164 



MARTINS 



Pedipes ovalis C. B. Adams, 1849 
Genus Creedonia new genus 

Creedonia succinea (Pfeiffer, 1 854) 
Genus Microtralia Dali, 1894 

Microtralia occidentalis (Pfeiffer, 1 854) 
Genus Leuconopsis Hutton, 1884 
Leuconopsis novimundi (Pilsbry & 

McGinty, 1949) 
Leuconopsis manningi new species 
Leuconopsis sp. 
Subfamily Melampinae Pfeiffer, 1853 
Genus Melampus Montfort, 1810 
Subgenus Metampus s.s. 
Melampus (Melampus) coffeus 

(Linnaeus, 1758) 
Melampus (Melampus) bidentatus Say, 
1822 
Subgenus Detracia Gray, 1840 
Melampus (Detracia) bullaoldes 

(Montagu, 1808) 
Melampus (Detracia) floridanus Pfeiffer, 

1856 
Melampus (Detracia) paranus (Morrison, 

1951) 
Melampus (Detracia) monile (Bruguière, 

1789) 
Melampus (Detracia) morrlsoni new 
name 
Genus 7"ra//a Gray, 1840 
Subgenus 7"ла//а s.s. 
7ra//a (Tralla) ovula (Bruguière, 1789) 
Conclusions 

Phylogeny and Classification 
Zoogeography of the Ellobiidae 
Acknowledgments 
Literature Cited 
Appendix 



INTRODUCTION 

The Ellobiidae are primitive pulnnonate 
gastropods that characterize the malaco- 
fauna of the upper and supra-littoral zones of 
the mangroves of the tropical regions and 
salt marshes of temperate regions. The Ello- 
biidae were first assigned familial rank by 
Lamarck (1809) when he included his Auric- 
ula [= Ellobium Röding], along with three 
other unrelated genera, within the "auricula- 
cées". Since then, several comprehensive 
works have been published. The group was 
illustrated in Reeve's Conchologia Systemat- 
ica (1842) and Conchologia Iconica (1877). 
A pictorial presentation was given in Martini 
& Chemnitz' Conctiylien-Cabinet by Küster 
(1844) and Kobelt (1897-1901). Pfeiffer 
(1854b) outlined a monograph of the Auricu- 
lacea [= Ellobiidae] in his Synopsis and fully 
developed the work in his IVIonograptiia in 
1856, which he revised and completed 



twenty years later. Odhner (1925) rearranged 
the classification of the family on the basis 
of radular morphology; Morton (1955c) in- 
cluded morphology of the stomach and re- 
productive organs in his review of the group. 
Only a few genera have received compre- 
hensive treatment. The genus Plecotrema 
[= Laemodonta Philippi] was first revised by 
H. & A. Adams (1853) and was studied by 
Sykes (1895) and, more recently, by Huben- 
dick (1956). The genera Ellobium Röding and 
Melampus Montfort were studied by H. & A. 
Adams (1854). Cox (1882) worked on the no- 
menclature and distributuion of Pytliia Röd- 
ing, and Connolly (1915) did a similar study 
on the genus Marinula King. Noteworthy are 
the detailed anatomical and histological 
studies on Melampus boholensis H. & A. Ad- 
ams (Koslowsky, 1933), Myosotella myosotis 
(Draparnaud) (Meyer, 1955; Morton, 1955b) 
and Auhculinella (L.) bidentata (Montagu) 
(Morton, 1955b). Marcus & Marcus (1965a, b) 
discussed the anatomy of Melampus (M.) 
coffeus (Linnaeus), Melampus (D.) paranus 
(Morrison), Ellobium (A.) dominicense (Férus- 
sac) and Blauneria tieterociita (Montagu). 
Giusti (1973) discussed the radula and anat- 
omy of Ovatella firminii (Payraudeau), and the 
shell, radula and anatomy of Myosotella my- 
osotis (Draparnaud) were dealt with by Giusti 
(1973, 1976) and Cesari (1973, 1976). 

The Western Atlantic ellobiids were in- 
cluded in the very earliest conchological re- 
ports of American scientists. Say (1822), the 
first New World malacologist, described the 
common Melampus (M.) bidentatus. Gould 
(1841) illustrated Say's species and Myoso- 
tella myosotis (Draparnaud), which is thought 
to have been introduced to North America 
from Europe. Study of American ellobiids 
was particularly influenced by Binney (1859, 
1865) and Dall (1885). Binney (1859) figured 
most of the common species; his later figures 
(1865) were copied by subsequent workers 
(Tryon, 1866; Dall, 1885, 1889; M. Smith, 
1937; Abbott, 1974), sometimes without crit- 
ical investigation. For example, Binney's in- 
accurate representation of Melampus (D.) flo- 
ridanus Pfeiffer in fact represents a dwarf 
Melampus (M.) bidentatus Say. 

Morrison (1 946, 1 951 a, 1 951 b, 1 954, 1 958, 
1959, 1964) addressed several aspects of 
American ellobiid systematics, life history 
and ecology, and Clench (1964) revised the 
Western Atlantic Pedipes and Laemodonta. 

The only detailed comprehensive anatom- 
ical research on Western Atlantic ellobiids 



WESTERN ATLANTIC ELLOBIIDAE 



165 



was that of Marcus & Marcus (1965a, b) on 
the four species mentioned above. Several 
aspects of the life history and anatomy of 
Melampus (M.) bidentatus Say have been 
investigated, almost exclusively in the New 
England area. Hausman (1932), Holle & 
Dineen (1957) and Grandy (1972) focused on 
various aspects of the ecology of this spe- 
cies, while Apley (1970) and Russell-Hunter 
et al. (1972) did extensive research on its 
early life history. Additional investigations 
have involved the morphology of the nervous 
system (Price, 1977; Kahan & Moffett, 1979), 
several aspects of physiology and behaviour 
(Price, 1979, 1980; Hilbish, 1981; Capaido, 
1983), locomotion (Moffett, 1979) and feed- 
ing (Thompson, 1984). 

In the present work particular attention has 
been paid to shell morphology, the radula 
and internal anatomy, especially the repro- 
ductive and nervous systems. This holistic 
approach helps to clarify the systematic po- 
sition and phylogenetic relationships of the 
Western Atlantic ellobiids. 



tioned above, included Azorean ellobiids 
from my own collection, specimens from Ma- 
laysia sent by A. Sasekumar and another se- 
ries of specimens from Hong Kong sent by B. 
S. Morton; all are now part of my collection. 
The British Museum (Natural History) has 
kindly allowed me to work on preserved 
specimens of Marinula. 

Most of the Western Atlantic species of el- 
lobiids were first studied and described by 
European scientists and much of the type 
material is thought to be in European muse- 
ums. Only the type material studied in brief 
visits to the British Museum (Natural History) 
and to the Muséum National d'Histoire Na- 
turelle de Paris, as well as that kindly sup- 
plied by the Muséum d'Histoire Naturelle de 
Genève, were incorporated in this work. 
Sherborn (1940) and Dance (1966) have been 
used to locate tentatively the collections that 
might contain required type material. 

Throughout the text, the museums and 
collections in which the studied material is 
deposited are indicated by the following ab- 
breviations: 



MATERIALS AND METHODS 



AMNH 



Materials ANSP 

Thousands of specimens from many local- BMNH 
ities were studied to understand inter- and 
intrapopulational variation in shell morphol- 
ogy. To accomplish this I studied the collec- R.B. 
tions at the Museum of Comparative Zool- 
ogy, Harvard University, Cambridge, at the 
American Museum of Natural History, New FMNH 
York, at the Academy of Natural Sciences of 
Philadelphia and at the United States Mu- LSL 
seum of Natural History, Washington, D. С A.M. 
Because museum collections were very poor 
in material with preserved soft tissue, the ma- 
jority of the internal anatomical work was 
done on specimens from my collections. MCZ 

Most of the Western Atlantic material was 
obtained during field trips along the Atlantic 
coast of the United States, to Bermuda, the MHNG 
Bahamas, Puerto Rico and Venezuela. Some 
specimens from R. С Bullock's collection MNHNP 
were also kindly made available to me. Field 
trips were very important in providing large NHMB 
series of most recorded species and in allow- 
ing examination of living animals in their hab- RAMM 
itats. Most of this material is now in my col- 
lection. USNM 

Material not from the Western Atlantic, be- 
sides that in the museum collections men- 



American Museum of Natural His- 
ton/. New York, NY, U.S.A. 
Academy of Natural Sciences of 
Philadelphia, PA, U.S.A. 
The Natural History Museum [for- 
merly British Museum (Natural His- 
tory)], London, U.K. 
Private collection of R. С Bullock, 
University of Rhode Island, King- 
ston, Rl, U.S.A. 

Field Museum of Natural History, 
Chicago, IL, U.S.A. 
Linnaean Society of London, U.K. 
Private collection of A. M. F. Mar- 
tins, University of the Azores, Ponta 
Delgada, Sao Miguel, Azores, POR- 
TUGAL. 

Museum of Comparative Zoology, 
Harvard University, Cambridge, 
MA, U.S.A. 

Muséum d'Histoire Naturelle de 
Genève, SWITZERLAND 
Muséum National d'Histoire Na- 
turelle de Paris, FRANCE 
Natural History Museum of Basel, 
SWITZERLAND 

Royal Albert Memorial Museum, 
London, U.K. 

National Museum of Natural History 
[formerly United States National 
Museum], Washington, DC, U.S.A. 



166 



MARTINS 



Methods 

Observation and Collection of Live Animals. 
Observations of external morphology were 
made In the field and in the laboratory. The 
animals were photographed with Koda- 
chrome film. Notes on the habitat were taken 
during collecting. 

Besides extensive search and collecting in 
a variety of habitats, six transects were made 
in January, 1981, in the mangroves of the 
Florida Keys. Duplicate transects were made 
in May, 1 982, at two of the 1 981 sites, one on 
the previously disturbed site, another adja- 
cent to it. All ellobiids found in the transects 
were collected and preserved. Qualitative 
analysis of this data is included in notes on 
habitats of the different species. 

Presen/ation. Most animals were immersed 
directly in 70% ethanol. Some were relaxed 
overnight in isotonic MgCl2 (75.2 g MgCls/l 
of distilled water) and then preserved in 70% 
ethanol. Some of the contracted and relaxed 
animals were fixed in Bouin's solution after 
the shell was cracked to allow better pene- 
tration of the fixative; others were frozen in 
fresh water for later dissection. This latter 
method seemed quite useful, because the or- 
gans maintained their original colors and 
softness, allowing easier dissection many 
months later. 

Measurements. Various numbers of speci- 
mens from different localities were selected 
(Table 1, Appendix). Shells and dissected re- 
productive systems were drawn using a Wild 
M8 microscope with drawing tube. All mea- 
surements were taken from these drawings 
using a GTCO digitizer and IBM microcom- 
puter. Radular teeth were counted from SEM 
photographs. 

Shell and Rad и la Preparations for Scanning 
Electron Microscope. Juveniles of most spe- 
cies and adults of the smaller species were 
mounted for SEM observation of the entire 
shell or the protoconch, or both. The shells 
were cleaned in 95%) ethanol in an ultrasonic 
cleaner for two to ten seconds, depending on 
the fragility of the specimen, and then were 
mounted on a stub with double-sided tape. 
The radulae were first cleaned in KOH (two 
pellets/10 ml distilled water), washed in dis- 
tilled water and in 70% ethanol. Ultrasonic 
cleaning was reduced to two seconds for 
each step. The radula was mounted on a 
piece of cover slip, to which it adhered when 
dry, and the cover slip was affixed to the stub 



with double-sided tape. The use of 70%) eth- 
anol alone had the advantage of slower evap- 
oration, which was preferable when small 
pieces had to be manipulated at the exact 
moment they dried, to ensure proper posi- 
tioning and good adhesion. I found very help- 
ful the use of human eyelashes attached to 
dissecting needles with "superglue." They 
are fine, flexible, but sufficiently hgid for 
clearing the membranes of the radula without 
tearing, and for facilitating positioning while 
mounting. 

All specimens were first coated with a sin- 
gle layer of carbon and then two layers of 
gold-palladium (60:40) in a Denton DV-502 
vacuum evaporator, and examined in an ISI 
MSM-3 SEM. 

Histology. Serial sections were made of 
specimens of every species collected. Some 
specimens were relaxed overnight in isotonic 
MgCl2 before fixation in Bouin's solution. For 
most of the specimens the shell was cracked 
and the pieces removed to allow better fixa- 
tion. 

Whole animals, dissected reproductive or- 
gans and stomach were embedded sepa- 
rately. Embedding was done with an Auto- 
technicon Duo, Model 2A. The specimens 
were dehydrated in S-29 and embedded in 
Paraplast. The blocks were refrigerated until 
sectioned. Sectioning was done with a Spen- 
cer 820 microtome. The thickness of the sec- 
tions varied from 8 to 15 |im. Best results 
were achieved by keeping the block and the 
blade refrigerated during sectioning. The 
preparations were stained with Heidenhain's 
aniline blue, following Luna (1968). 



ABBREVIATIONS USED IN FIGURES 



aa 


antenor aorta 


acpn 


anterior cutaneous pedal nerve 


ad 


anterior diverticulum 


adgl 


anterior lobe of digestive gland 


agi 


albumen gland 


al 


aperture length 


ain 


anterior labial nerve 


alpn 


anterolateral pedal nerve 


amgl 


anterior mucous gland 


ampn 


anteromedial pedal nerve 


an 


aortic nerve 


angi 


anal gland 


ann 


anal nerve 


aoen 


anterior esophageal nerve 


au 


auricle 



WESTERN ATLANTIC ELLOBIIDAE 



167 



avd 


anterior vas deferens 


ot 


ovotestis 


aw 


aperture width 


P 


propodium 


bb 


buccal bulb 


pa 


posterior artery 


be 


buccal commissure 


pc 


pedal commissure 


bg 


buccal ganglion 


pepn 


posterior cutaneous pedal nerve 


br 


bursa 


pevn 


posterior cutaneous visceral nerve 


brd 


bursa duet 


pd 


posterior diverticulum 


bw 


body whorl 


pdgl 


posterior lobe of digestive gland 


bwl 


body whorl length 


pe 


penis 


С 


central tooth 


pee 


pericardium 


ca 


gastric caecum 


pen 


penial nerve 


car 


cardiac region of stomach 


per 


penial retractor muscle 


cbc 


eerebrobueeal connective 


pg 


pedal ganglion 


ce 


cerebral commissure 


pgi 


palliai gland 


cg 


cerebral ganglion 


phmn 


pharyngeal retractor muscle nerve 


clpin 


cutaneous-lateral pleural nerve 


phn 


pharyngeal nerve 


cm 


eolumellar muscle 


pig 


pleural ganglion 


cmn 


columellar muscle nerve 


pin 


posterior lip nerve 


cpc 


cerebropedal connective 


pipe 


pleuropedal connective 


epic 


eerebropleural connective 


pipn 


posterior lateral pedal nerve 


er 


crop 


piprc 


pleuroparietal connective 


et 


columellar tooth 


pmgl 


posterior mucous gland 


ctw 


eolumellar tooth width 


pmpn 


posteromedial pedal nerve 


div 


penial diverticulum 


pn 


pneumostome 


e 


eye 


pnn 


pneumostomal nerve 


epan 


external palliai nerve 


poen 


posterior esophageal nen/e 


ev 


elbow of vagina 


PPni 


first posterior pedal nen/e 


f 


foot 


РРП2 


second posterior pedal nerve 


fgo 


female genital opening 


Pr 


prostate gland 


fp 


fertilization pouch 


pren 


parietocutaneous nerve 


gn 


genital nerve 


prg 


parietal ganglion 


hd 


hermaphroditic duct 


prgi 


anterior left parietal ganglion 


hgl 


hypobranchial gland 


prg2 


posterior left parietal ganglion 




intestine 


prve 


parietovisceral connective 


il 


inner lip 


Pti 


anterior parietal tooth 


ipan 


internal palliai nerve 


Pt2 


posterior parietal tooth 


к 


kidney 


ptn 


peritentacular nerve 


kp 


kidney pore 


ptw 


width of posterior parietal tooth 


L 


lateral teeth 


pv 


pulmonary vein 


ipgi 


lower pneumostomal gland 


pvd 


posterior vas deferens 


M 


marginal teeth 


pyl 


pyloric region of stomach 


m 


mantle skirt 


r 


rectum 


man 


mantle skirt artery nerve 


rb 


riblets 


mb 


muscular band 


rme 


roof of mantle cavity 


mgl 


mucous gland 


s 


stomach 


ml 


mantle lappet 


sgl 


salivary gland 


min 


medial lip nerve 


sgin 


salivary gland nerve 


mo 


mantle organ 


sh 


shoulder of body whorl 


mpan 


medial palliai nerve 


si 


shell length 


ms 


muscular strand of stomach 


spe 


subpedal commissure 


mv 


mantle skirt vein 


spov 


spermoviduct 


nn 


nuchal nerve 


sr 


spire 


ce 


esophagus 


srI 


spire length 


og 


osphradial ganglion 


St 


statocyst 


Ol 


outer lip 


stn 


statocyst nerve 


on 


ocular nerve 


sv 


seminal vesicle 


osg 


open spermatic groove 


sw 


shell width 



168 




MARTINS 


Т 


transitional teeth 




t 


tentacle 


sr^ 


tcm 


tentacular control muscle 


sh. 


tn 


tentacular nerve 


upe 
upgl 


unwrapped penis 

upper pneunnostomal gland 


bw_ 


V 

ve 


vagina 
ventricle 


Pt2. 


vg 


visceral ganglion 


Pt1- 


wpe 


wrapped penis 


A ~ 




TAXONOMIC CHARACTERS 



FIG. 1. Conchological characters. A, Shell termi- 
nology; B, Morphometry. 



Mayr (1969: 121) stated, "A taxonomic 
character is any attribute of a member of a 
taxon by which it differs or may differ from a 
member of a different taxon." Application of 
this definition cannot be uniform and gener- 
alized. Although there is consensus that a ho- 
listic approach is essential to sound classifi- 
cation (Mayr, 1969; Solem, 1978), one must 
be aware of the difference between charac- 
ters used at the species level or even for ge- 
neric grouping and those used for higher taxa. 
Characters that stress differences are used to 
define lower taxa, whereas those characters 
sensitive to convergence and seemingly less 
affected by environmental factors are used to 
define phylogenetic relationships among 
higher taxa. For example, the pattern of the 
spiral grooves on the shell is useful in sepa- 
rating Melampus (M.) coffeus from Melampus 
(M.) bidentatus, whereas the arrangements of 
the nervous and reproductive systems are the 
most consistent characters in defining the 
subfamilies of the Ellobiidae. In the Ellobiidae 
the shell and radular morphology are useful 
mostly at the generic or specific level. Harry 
(1951) and Hubendick (1978) pointed out the 
value of anatomical studies for clarifying tax- 
onomic relationships within the group. Morton 
(1955c), followed by Marcus (1965) and Mar- 
cus & Marcus (1965a, b), adopted this holistic 
approach by including analyses of the stom- 
ach and reproductive organs; this approach 
led to somewhat surprising results, such as 
inclusion of Auriculinella and Blauneria within 
the Ellobiinae. 

In the present study conchological, radular 
and anatomical characters are used. Each of 
these different characters will now be con- 
sidered in more detail. 



Conchological Characters (Fig. 1) 

The shell, more than other molluscan 
structures, has the obvious advantages of 
permanence and ease of study. Traditionally 
it has been the important basis for distinc- 
tion of most taxa (Zilch, 1959). Application of 
mathematical models and statistical analyses 
has provided tools for the interpretation of 
shell morphometry with accuracy and preci- 
sion (Sokal & Sneath, 1963). Mathematical 
analysis of geometry of shell coiling has also 
been used (Raup, 1961, 1962, 1966, 1967; 
Raup & Michelson 1965; Rex & Boss, 1976; 
Warburton, 1979; Harasewych, 1981). This 
method aims at providing an opportunity for 
interpretation of evolutionary changes in shell 
morphology in functional terms and as an in- 
dication of strategies of adaptation to differ- 
ent habitats (Vermeij, 1971). Such interpreta- 
tion has been challenged recently (Gould, 
1984). In spite of modern refinements in anal- 
yses of conchological characters, it remains 
true that some, such as shell shape, have 
limited weight in assessing phylogenetic re- 
lationships because shell morphology is of- 
ten strongly influenced by diverse environ- 
mental parameters (Hubendick, 1978; Solem, 
1978). 

Other shell characters, such as the proto- 
conch, resorption of the inner whorls and ap- 
ertural dentition, demonstrate more nearly 
constant patterns and are useful at the spe- 
cific and even generic level. 

The gastropod protoconch indicates the 
type of larval development that organisms in 
the different groups have undergone (Dall, 
1924; Lutz et al., 1984). It might also have 
other very distinctive features that make it a 



WESTERN ATLANTIC ELLOBIIDAE 



169 



useful taxonomic character (Walter, 1962; 
Beuchet & Waren, 1980; Turner & Lutz, 
1984). Study of the protoconch has been 
aided greatly by the use of the scanning elec- 
tron microscope, an increasingly important 
tool in malacology (Solem, 1970; Calloway & 
Turner, 1978). The SEM has been used to 
examine small and juvenile specimens, and 
to study the external morphology of the shell, 
radula and larvae. In this study the SEM was 
used to examine the protoconchs and radu- 
lae of most of the Western Atlantic ellobiids, 
and to provide photomicrographs of small 
and juvenile specimens. 

Ellobiid protoconch morphology proved a 
very useful taxonomic character in most 
cases. The Melampinae, for example, have 
only one type of heterostrophic protoconch, 
which shows one-half of each nuclear whorl. 
This feature might reflect the fact that, as far 
as is known, all have free-swimming larvae. 
Indeed, a similar type of protoconch occurs 
in Pyramldellidae having larvae with a long 
pelagic phase (Haszprunar, 1985). The mor- 
phology of the protoconch in the other sub- 
families of the Ellobiidae does not show an 
exclusive subfamilial pattern. For example, all 
the Pythiinae, Ellobiinae and the pedipedin- 
ian genera Pedipes and Creedonia have a 
bulbous protoconch with an umbilicus and a 
laterally facing aperture. The protoconch of 
the pedipedinian genera Microtralia and 
Pseudomelampus sits atop the teleoconch 
with the aperture facing the columellar axis, 
as in the Melampinae, rather than laterally as 
in all pythiinians and ellobiinians. Particular 
anatomical features indicate that these two 
genera belong to the Pedipedinae, however. 
The protoconch is very uniform within a spe- 
cies and, in the case of the West Indian Pe- 
dipes, it was the only consistent diagnostic 
conchological character that allowed clear 
separation of species. 

Shell resorption, as seen in the Ellobiidae, 
also occurs in the Neritacea, Helicinidae and 
Conidae. It was first noted by Montagu (1 803; 
235) in his Voluta denticulata [= Myosotella 
myosotis (Draparnaud)] and was reported for 
most members of the Ellobiidae by Gray 
(1840; 220-221). Crosse & Fischer (1879, 
1882), however, studied the phenomenon in 
more detail and are usually credited with its 
discovery. Resorption of the inner whorls pro- 
vides a larger cavity in which the organs of the 
visceral mass can be rearranged with spatial 
economy. For example, in Melampus and Mi- 
crotralia, which show a high degree of resorp- 



tion, the conspicuous ovotestis has moved to 
an apical position and displaced the posterior 
lobe of the digestive gland; in Pedipes and 
Creedonia, which do not resorb the inner 
whorls, the ovotestis lies embedded in the 
apical, conspicuous posterior lobe of the di- 
gestive gland. This character varies within the 
different subfamilies of the Ellobiidae, but can 
be useful at lower taxonomic levels. In Melam- 
pus s.S., for example, the partition of the inner 
whorls occupies only one-fourth of the body 
whorl (Figs. 225, 267), whereas in the subge- 
nus Detracia it occupies at least three-fourths 
of the body whorl (Figs. 302, 316). The ex- 
treme case of variation within one subfamily 
occurs in the Pedipedinae, in which Pedipes 
and Creedonia completely retain the inner 
whorls (Figs. 106, 128, 153), whereas in Mi- 
crotralia resorption reaches the most ad- 
vanced stage in the Ellobiidae with less than 
a quarter of the interior partitions left (Fig. 
178). In conjunction with other features, the 
lack of shell resorption justified the creation of 
the new genus Creedonia. The degree of re- 
sorption also supported the separation of De- 
tracia as a subgenus oi Melampus s.l. and was 
helpful in the interpretation of some anatom- 
ical differences observed between that sub- 
genus and Melampus s.s. 

Apertural dentition, an important character 
in gastropod classification, is a conspicuous 
feature of the Ellobiidae. One of the most 
commonly accepted functions of the aper- 
tural dentition is that of constituting a barrier 
against predators. From my observations on 
the disposition of the various branches of the 
columellar muscles along the conspicuous 
internal lamellae of Melampus (D.) bullaoides 
(Fig. 302), I think that this feature also helps 
in positioning the shell during locomotion. 
Although variable, there are some general 
patterns of apertural dentition. On this basis 
one can characterize broadly the different 
subfamilies as follows; Ellobiinae with bipli- 
cate inner lip, with columellar and parietal 
teeth very close together; Pythiinae with 
evenly spaced triplicate inner lip with first pa- 
rietal tooth strongest; Pedipedinae with two 
columellar teeth and strong parietal tooth; 
Melampinae with inner lip dentition restricted 
to anterior half, columellar and posterior pa- 
rietal teeth conspicuous, outer lip dentate. 
There are exceptions to these patterns, how- 
ever, for the species in the melampinian genus 
Tralla have an inner lip structure very similar to 
that of the pythiinian genus Myosotella. The 
inner lip dentition of Microtralia deviates from 



170 



MARTINS 




FIG. 2. Terminology for radular teeth of Melampus 
(M.) coffeus. A, Top view of central tooth; B, Top 
view of first lateral tooth; C, Lateral view of first 
lateral tooth; D, Top view of tenth marginal tooth; 
E, Top view of 20th marginal tooth. 



the pattern of the Pedipedinae in having only 
one columellar tooth. The apertural structure 
of the pythiinian genera Cylindrotis and Au- 
riculastra resembles that of the Ellobiinae and 
Ellobium (E.) aurisjudae has a conspicuous 
posterior parietal tooth. 

Radular characters 

The molluscan radula is a valuable charac- 
ter in the classification of higher taxa and is 
the basis of phylogenies proposed for the 
Gastropoda (Gray, 1853; Troschel, 1856- 
1 893; Mörch, 1 867). Some authors have stud- 
ied ellobiid radulae in an attempt to divide the 
Ellobiidae into subfamilies. Classifications of 
the ellobiids by Odhner (1925) and Thiele 
(1 931 ) were based mainly on radular morphol- 
ogy, but these authors differed in their sub- 
familial division. Odhner adopted six subfam- 
ilies whereas Thiele recognized only three. 
Observation of the radula with a light micro- 
scope provides only limited information on the 
intricate articulation of the different teeth with 
one another (Figs. 250, 395). The SEM opened 
new vistas in the study of radular morphology 
and function (Solem, 1972b, 1974). 

The terminology used in this study follows 
that of Fretter & Graham (1962) and Ober- 
holzer et al. (1970) (Fig. 2). The radula of the 
ellobiids characteristically has many teeth in 
each row; the central tooth usually has a 
small crown. In most species the transition 
from the lateral teeth, which have a strong 



mesocone, to the pectinate marginal teeth is 
gradual. Morphology of the radula in the 
Melampinae and Ellobiinae is rather uniform, 
but it varies in the Pedipedinae and Pythiinae. 
The radula of the Melampinae undergoes a 
series of morphological changes with age. 
The deeply indented crown of the lateral 
teeth of very young individuals becomes the 
unicuspid, triangular crown of adults. Some 
species, however, seem to have a radula with 
neotenic features, for example Melampus (D.) 
floridanus and Melampus (D.) paranus, which, 
as adults, have a conspicuous ectocone on 
the lateral teeth. This structure, present in the 
radula of the juveniles of some species of the 
Melampinae (Figs. 243-249, 370, 371), disap- 
pears with age. Marcus & Marcus (1963, fig. 
8) observed the same morphological change 
in the radula of Ellobium (A.) domlnicense. 
Their illustration of the radula of a very young 
specimen of that species shows a striking 
resemblance to the radula of an adult Blaune- 
ria heteroclita. 

The Pedipedinae and Pythiinae display 
great radular diversity with as many as three 
radular types in each subfamily. Radulae of 
some Pedipedinae, such as Microtralia, re- 
semble that of the Melampinae, whereas in 
the Pythiinae the strong mesocone on the 
radular teeth of Cassidula and Pythia resem- 
bles that in adult Ellobium. 

The radula of the ellobiids is a much more 
useful character at the generic level than at 
the specific level. The minute differences in 
the radulae developed by analysis of closely 
related pairs such as Melampus (M.) cof- 
feus — Melampus (M.) bidentatus, Pedipes 
mirabilis — Pedipes ovalis and Leuconopsis 
novimundl — Leuconopsis manningi failed to 
provide morphological evidence useful in the 
separation of these species pairs. On the 
other hand, the different genera, mainly within 
the subfamilies Pythiinae and Pedipedinae, 
are readily distinguished on the basis of their 
radular morphology. 

Anatomical characters 

A series of anatomical characters com- 
monly used in devising classifications was 
listed by Solem (1978). Because all charac- 
ters do not have the same taxonomic value 
weighting always must be applied. Those 
characters having greater influence on the 
cohesion of the group should be used in phy- 
logenetic studies. Those same characters 
should be the least affected by nongenetic 



WESTERN ATLANTIC ELLOBIIDAE 



171 



factors, such as environmental and com- 
petitive pressures, exemplified by habitat 
and food. Thus the reproductive and the ner- 
vous systems ought to be considered prime 
taxonomic characters for the interpretation 
of phylogenetic relationships among higher 
taxa. 

Stomach: Graham's comprehensive studies 
(1939, 1949) of the functional morphology of 
the molluscan stomach showed an evolution- 
ary trend toward the disappearance of the 
crystalline style and simplification of the sort- 
ing areas in conjunction with the adoption of 
a macrophagous carnivorous diet. He ob- 
served the forward migration of the cardiac 
opening, with consequent reduction of the 
stomach to a blind sac into which the diges- 
tive gland discharges, and the increase in the 
muscularity of the mid-section to form a giz- 
zard. 

It is generally recognized that the basom- 
matophoran stomach originated from the 
prosobranch condition and it appears to me 
that it evolved along two different lines. The 
lower basommatophoran or archaeopulmo- 
nate stomach shows a tendency toward a 
forward migration of the cardiac opening. 
Otina Otis (Turton), a primitive marine pulmo- 
nate, retains a vestigial style sac and has a 
rudimentary gizzard (Morton, 1955a). In the 
higher, limnic basommatophorans the stom- 
ach remains open-ended, with esophageal 
and intestinal openings at opposite ends, as 
shown in Carhker (1946) and Morton (1955c). 
In this group the simplest stomach occurs in 
Acroloxus, which lacks musculature, has a 
well-developed caecum similar to a style sac 
and a structure similar to a crystalline style 
(Hubendick, 1978). Morton (1952, 1953) also 
investigated the functional morphology of the 
gastropod stomach and, on the basis of the 
disposition of the internal ciliary patches and 
of the tendency toward stronger muscularity 
of the mid-section, used it as a character in 
the classification of the ellobiids (Morton, 
1955c). 

In this study only the external appearance 
of the stomach was noted. Without an under- 
standing of the functional morphology of the 
internal parts, phylogenetic inferences and 
use in classification would be unwarranted 
and possibly misleading. 

Reproductive System: Traditionally the mol- 
luscan reproductive system has been ac- 
corded special value in the understanding of 
the phylogenetic relationships among higher 



taxa (Duncan, 1960a, b; Visser, 1977, 1981; 
Gosliner, 1981; Haszprunar, 1985, 1988; Sal- 
vini-Plawén & Haszprunar, 1987). The impor- 
tance of the reproductive system in gastro- 
pod evolutionary studies is corroborated by 
my studies. 

A basic plan of the gastropod reproduc- 
tive system consists of a posteriorly located 
gonad, a middle glandular section and an 
anterior duct associated with the palliai re- 
gion, primitively glandular owing to its prob- 
able origin from the hypobranchial gland 
(Fretter, 1984). This simple tube becomes in- 
creasingly complex with the appearance of 
specialized evaginations and of the herma- 
phroditic condition (Ghiselin, 1966). In proso- 
branchs gonochorism is the rule, a condition 
currently considered primitive (Haszprunar, 
1988). Cases of protandry and of simulta- 
neous hermaphroditism exist in archaeo- 
gastropods and mesogastropods, however 
(Fretter, 1946). Simroth (1907) and Huben- 
dick (1945) both thought that hermaphrodit- 
ism was the original condition among the gas- 
tropods. Krull (1935, fide Fretter & Graham, 
1962) also shared Simroth's view and, based 
on the fact that the palliai oviduct of the 
prosobranch hydrobiids is divided in a man- 
ner similar to that of the monaulic pulmo- 
nates (species with one bisexual duct), he 
suggested that the hydrobiids were the most 
primitive gastropods. This view has not been 
accepted by later authors. In the euthy- 
neurans (opisthobranchs and pulmonates), 
once commonly thought to have evolved from 
the archaeogastropods (Pelseneer, 1894a; 
Hubendick, 1945; Morton, 1955c), but more 
probably from the mesogastropods (Fretter, 
1946; Boettger, 1954; Duncan, 1960a; Gos- 
liner, 1981)orApogastropoda(Salvini-Plawén 
& Haszprunar, 1987; Haszprunar, 1988), her- 
maphroditism is the universal condition (Ghis- 
elin, 1969). Opinions also differ as to which of 
the two hermaphroditic conditions appeared 
first, monaulic (one bisexual duct) or diaulic 
(two separate sexual ducts). Pelseneer's sug- 
gestion (1894b: 19) that hermaphroditism in 
mollusks arose by the secondary addition or 
grafting of a male system to the female indi- 
vidual has led to the view that monauly is the 
primitive condition (Ghiselin, 1966; Marcus & 
Marcus, 1965b; Visser, 1977, 1981; Huben- 
dick, 1978). Solem (1972a, 1978) considered 
diauly the primitive condition, however, and 
stated that partial or total fusion of the male 
and female reproductive tracts has evolved 
independently in several groups. The choice 



172 



MARTINS 



of one or another hypothesis has obvious 
phylogenetic implications for the use of the 
reproductive system. Visser (1981) rejected 
Solem's opinion because there is no evidence 
of two separate gonads with two separate 
gonoducts in primitive gastropods. Visser, in 
contrast to Pelseneer, stated that hermaph- 
roditism in the Basommatophora, unlike that 
of the Stylommatophora, was derived from a 
male prosobranch. As evidence he cited the 
consistency of the penial structure throughout 
the basommatophorans (see also Hubendick, 
1978). 

My work has led me to support the most 
commonly held view, namely that monauly 
and a glandular palliai gonoduct represent 
the primitive condition. The tendency toward 
reduction of the glandular elements of the re- 
productive system to the proximal, nonpallial 
portion is hereby taken as a derived trend. 
Supporting this view is the presence of glan- 
dular palliai gonoducts among littorinids and 
the primitive opisthobranchs (Gosliner, 1 981 ). 
Existence of such glandular ducts in groups 
otherwise clearly primitive (Pythiinae, Ellobii- 
nae) also is taken as supportive circumstan- 
cial evidence for the case. 

The terminology used in this study follows 
that of Duncan (1975), Visser (1977), Berry 
(1977) and Tompa (1984). Histological stud- 
ies were carried out to clarify some critical 
features of basic morphology, such as the 
extent of the mucous and prostate glands 
and to establish the aulic condition, the site 
of separation of male and female ducts. No 
distinction was made between the different 
components of the penial complex (penial 
sheath, preputium and penis) and this entire 
structure is herein called the penis. The de- 
gree of adhesion of the anterior vas deferens 
to the penis is also considered, the free con- 
dition being interpreted as derived. 

Central Nervous System. Use of the pulmo- 
nate central nervous system as a primary tax- 
onomic character has become increasingly 
accepted (Bargmann 1930; Van Mol, 1967; 
Bishop, 1978, Haszprunar, 1985, 1988; Sal- 
vini-Plawén & Haszprunar, 1987). Morton 
(1955c) and Regondeau et al. (1976) agreed 
that within the gastropods concentration of 
the ganglia is a derived character, but Morton 
shared Fretter & Graham's concern (1949) 
that sole reliance on characters of the ner- 
vous system to establish phylogenetic rela- 
tionships can be misleading. Haszprunar 
(1985, 1988) emphasized the possibility that 



concentration of ganglia and consequent eu- 
thyneury could be associated with small size 
in some cases. 

The degree of concentration of the ganglia 
of the central nervous system is considered 
important because the complexity of an en- 
tire system is generally unaffected by envi- 
ronmental pressures. Any major change in 
the arrangement of the ganglia probably 
would mean a greater rearrangement at most 
levels of anatomical organization. For this 
reason the morphology of the central nervous 
system is considered herein to be a taxo- 
nomic character useful at higher levels of 
classification. 

A detailed treatment of the ellobiid central 
nervous system is provided for Ellobium (A.) 
dominicense (Fig. 21) and Melampus (M.) 
coffeus (Fig. 255). The terminology adopted 
here is from several sources (Simroth 1912, 
1925-1928; Bargmann, 1930; Carhker, 1946; 
Brisson, 1963; Price, 1977). For most species 
only the relative concentration of the ganglia 
seemed important, but the nerves were 
found to approximate the pattern in Melam- 
pus (M.) coffeus. 



CLASSIFICATION OUTLINE, WESTERN 
ATLANTIC ELLOBIIDAE 

Family Ellobiidae H. & A. Adams in Pfeiffer, 1854 
Subfamily Ellobiinae H. & A. Adams In Pfeiffer, 
1854 

Genus Ellobium Röding, 1798 
Subgenus Auncu/oc/es Strand, 1928 
Ellobium (A.) dominicense (Férussac, 
1821) 
Genus Blauneria Shuttleworth, 1854 

Blauneria heteroclita (Montagu, 1808) 
Subfamily Pythiinae Odhner, 1925 
Genus Myosotella Monterosato, 1906 

Myosotella myosotis (Draparnaud, 1801) 
Genus Laemodonta Philippi, 1846 

Laemodonta cubensis (Pfeiffer, 1854) 
Subfamily Pedipedinae Fischer & Crosse, 1880 
Genus Pedipes Scopoli, 1777 

Pedipes mirabilis (Mühlfeld, 1816) 
Pedipes ovalis С В. Adams, 1849 
Genus Creedonia new genus 

Creedonia succinea (Pfeiffer, 1 854) 
Genus Microtralia Dall, 1894 

Microtralia occidentalis (Pfeiffer, 1 854) 
Genus Leuconopsis Hutton, 1884 
Leuconopsis novimundi (Pilsbry & 

McGinty, 1949) 
Leuconopsis manningi new species 
Leuconopsis sp. 
Subfamily Melampinae Stimpson, 1851 



WESTERN ATLANTIC ELLOBIIDAE 



173 



Genus Melampus Montfort, 1810 
Subgenus Melampus s. s. 
Melampus (M.) coffeus (Linnaeus, 1758) 
Melampus (M.) bidentatus Say, 1 822 
Subgenus Detracia Gray in Turton, 1840 
Melampus (D.) bullaoides (Montagu, 

1808) 
Melampus (D.) floridanus (Pfeiffer, 1 856) 
Melampus (D.) paranus (Morrison, 1951) 
Melampus (D.) monile (Bruguière, 1789) 
Melampus (D.) morrisoni new name 
Genus Tralla Gray in Turton, 1840 
Subgenus Tralla s.S. 
Tralla (T.) ovula (Bruguière, 1 789) 



SYSTEMATICS 

Family Ellobiidae H. & A. Adams in Pfeiffer, 
1854 

Auriculidae Lamarck, 1809: 321 [corrected 
from "Les Auhculacées" by Gray, 1840]. 

Auriculae Lamarck. Férussac, 1821: 32. 

Auriculadae Lamarck. Gray, 1824: 107. 

Auriculacea Lamarck. Blainville, 1824: 245. 

Auriculaceae Lamarck. Menke, 1828: 19. 

Auhculoidea Lamarck. Cristofori & Jan, 
1832: 6. 

Auriculidea Lamarck. Beck, 1837: 101. 

Auhculata Lamarck. Sismonda, 1842: 26. 

Auriculiadae Lamarck. De Kay, 1843: 57. 

Auriculina Lamarck. Agassiz, 1847: 41 [cor- 
rection for Auriculacea]. Non Grateloup, 
1838, nee Gray, 1847a. 

Carychiadae (Leach MS) Gray, 1847b: 269. 

Auhculae'inae Lamarck. Strobel, 1850: 32. 

Conovulidae Clark, 1850: 444. 

Melampidae Stimpson, 1851: 51. 

Ellobiidae H. & A. Adams in Pfeiffer, 1854b: 
146 [in synonymy with Auriculacea La- 
marck]. 

Description: Shell spiral, dextral (except in 
Blauneha), oval-conic, sometimes umbili- 
cate, smooth or with spiral sculpture, cov- 
ered with brownish periostracum; aperture 
elongate, round at base, angulate posteriorly, 
with strong folds on inner lip, outer lip sharp 
or weakly reflected, often dentate. Inner 
whorls resorbed (except in Pedipes and 
Creedonia). Protoconch heterostrophic. 

Animal completely retractable into shell. 
Head separated from foot by transverse 
groove, into which a large mucous gland 
opens. Operculum present in embryos, ab- 
sent in adults. Mouth T-shaped; horny upper 
jaw sometimes with folded extremities lining 
lateral lips; one pair of subcylindric, contrac- 



tile or subretractile tentacles; eyes sessile, 
medial to base of tentacles; foot long, ante- 
riorly blunt, sometimes transversely divided, 
posteriorly tapered and entire or bifid; pneu- 
mostome on right side, medial to anal aper- 
ture. 

Radula broad, elongate; teeth numerous; 
central tooth equilateral; lateral teeth inequi- 
lateral, becoming shorter toward outer edges 
of radula, abruptly or gradually changing into 
marginal teeth. 

Digestive system moderately long; salivary 
glands usually elongate; esophagus long, 
thin walled, longitudinally grooved, opening 
posteriorly into wide crop; stomach generally 
tripartite with thin-walled cardiac region, 
muscular medial and pyloric regions and 
thin-walled, smaller posterior caecum; diges- 
tive gland usually bilobed, emptying anteri- 
orly at crop, posteriorly at gastric caecum. 

Reproductive system hermaphroditic; ovo- 
testis acinose and embedded in digestive 
gland or leaf-like and covering part of stom- 
ach; hermaphroditic duct with generally con- 
voluted seminal vesicle; glandular complex 
composed of whitish albumen gland, convo- 
luted posterior mucous gland, straight ante- 
rior mucous gland and prostate gland cover- 
ing palliai ducts (except in Melampinae); 
fertilization chamber follows posterior mu- 
cous gland and gives rise to oviduct and 
spermiduct, which might or might not be 
completely separate for their entire length; 
bursa duct and bursa arising from vagina at 
variable distances from aperture; female ap- 
erture medial to pneumostome, anterior to 
union of mantle with neck; male aperture on 
right corner of cephalic groove, under right 
tentacle; a fold of skin (sperm groove) runs 
from near female to male aperture, functional 
only in Pythia; in all others the vas deferens 
lies embedded in neck skin; it separates from 
skin inward near male aperture and enters 
penis at posterior end; penial complex (penis 
and penial sheath) lying over buccal bulb and 
cerebral ganglia. 

The hypoathroid, pentaganglionate central 
nervous system is of the basommatophoran 
type (Bargmann, 1930; Haszprunar, 1985), 
composed of 1 1 discrete ganglia, joined by 
connectives of various lengths: paired cere- 
bral, buccal, pleural, parietal and pedal gan- 
glia, and an unpaired visceral ganglion. 

Remarks: The Ellobiidae were first assigned 
familial rank by Lamarck (1809) under the 
vernacular Les Auhculacées. The group in- 



174 



MARTINS 



eluded Lamarck's Auricula and three other 
genera (Melanopsis, Melania and Limnaea) 
that were assigned subsequently by other 
authors to different families. Many incorrect 
Latinizations of Lamarck's vernacular name 
followed; Blainville's (1824) Auriculacea be- 
came well established and was used in major 
monographs on the family (Reeve, 1842; 
Küster, 1844; Pfeiffer, 1856a, 1876; Kobelt, 
1898). 

The correct Latin designation, Auriculidae, 
was first used by Gray (1 840) and was widely 
accepted until the 1920s, when the names 
Ellobiidae H. & A. Adams in Pfeiffer, 1854, 
and Melampidae Stimpson, 1851, replaced 
Lamarck's name. 

According to the International Code of 
Zoological Nomenclature Art. 1 1 (e) the name 
Auriculidae has priority because, when first 
published, it was based upon the name then 
valid for the contained genus Auricula La- 
marck. Odhner (1925), however, preferred 
the name Ellobiidae H. & A. Adams because 
the type genus. Auricula Lamarck, 1799, is a 
synonym of Elloblum Röding, 1798. The 
name Ellobiidae has been in general use 
since that time. Works dealing exclusively 
with the family, such as those of Odhner 
(1925), Morton (1955b, c), Hubendick (1956), 
Clench (1964), Marcus (1965), Marcus & Mar- 
cus (1965a, b), Cesari (1973, 1976), or gen- 
eral ones, such as those of Thiele (1931), 
Zilch (1959), Hyman (1967), Franc (1968), 
Fretter (1975), Jones (1975), Runham (1975), 
Berry (1 977), Hubendick (1 978), Solem (1 978, 
1985), Boss (1982) and Haszprunar (1985, 
1988), and even popular books, such as 
those of Morns (1973), Humphrey (1975), 
Emerson & Jacobson (1976) and Rehder 
(1 981 ), are the most obvious examples of the 
acceptance of the name Ellobiidae. 

Recently the name Melampidae Stimpson, 
1851, has appeared in some influential mal- 
acological works, such as those of Keen 
(1971), Abbott (1974), Rios (1975) and Kay 
(1979). Morrison's reintroduction (1964) of 
the name Melampidae was unfortunate in 
several ways. It was an unnecessary distur- 
bance of taxonomic stability, because the 
name Ellobiidae had already been universally 
accepted. It also required a change to a dif- 
ferent type genus for the family. The appear- 
ance of the term Melampidae in influential 
malacological works obviously was leading 
to widespread use and consequent renewed 
taxonomic confusion. 

Strict application of the law of priority to 



family-group names would upset general use 
of the name Ellobiidae. In accordance with 
Art. 23 (d) of the ICZN, a petition should be 
submitted to the International Commission 
on Zoological Nomenclature to place the 
name Ellobiidae on the Official List of Family- 
Group Names in Zoology, and to place the 
names Auriculidae and Melampidae on the 
Official List of Rejected Names. 

Credit usually is given to H. & A. Adams 
(1855b) for the introduction of the name El- 
lobiidae. However, Pfeiffer (1854b), who had 
access to the Adams brothers' manuscript, 
referred to the to-be-proposed family name, 
but continued to use the name Auriculacea. 
For this reason the name Ellobiidae, which 
should be credited to H. & A. Adams, must 
take the date 1854, when it was first pub- 
lished by Pfeiffer as a synonym. 

The family Ellobiidae varies greatly in mor- 
phology and anatomy, but it is nevertheless 
readily identifiable as a group at the familial 
level. Starobogatov (1976) exaggerated the 
differences in the reproductive system and 
raised the family name to ordinal status and 
considered existing subfamilies separate 
families. This view has not gained accep- 
tance and I have concluded that the differ- 
ences within the ellobiids are reconcilable 
within a single family. 

Odhner (1925), using radular characters, 
and Zilch (1959), using shell morphology, 
recognized six subfamilies, Carychiinae, Mel- 
ampinae, Pedipedinae, Pythiinae, Cassiduli- 
nae and Ellobiinae. Morton (1955c) and Hu- 
bendick (1978) merged the Cassidulinae with 
the Pythiinae on the basis of the similarities of 
their reproductive systems, and assigned the 
latter name to the group. My studies support 
Morton's conclusions and I have followed his 
scheme of classification for the division of the 
Ellobiidae into subfamilies. 

Zilch (1959) recognized 20 genera of living 
halophilic ellobiids. Zilch's classification is 
accepted here with certain modifications and 
21 genera are recognized in this paper. Zilch 
considered Sarnia H. & A. Adams a subgenus 
of Tralla Gray, but Marincovich (1973), on the 
basis of radular morphology, placed it in the 
Ellobiinae. Sarnia (Fig. 181) shows strong 
conchological similarity to Pseudomelampus 
and Microtralia, and for that reason I include 
it in the Pedipedinae. Further information on 
the reproductive and nervous systems is 
needed to confirm the systematic position of 
this genus, however. I have synonymized 
herein Apodosis Pilsbry & McGinty with Leu- 



PYTHIINAE 



WESTERN ATLANTIC ELLOBIIDAE 175 

ELLOBIINAE CARYCHIINAE PEDIPEDINAE MELAMPINAE 




FIG. 3. Pictorial review of subfamilies of Ellobiidae, from most primitive to most advanced. A, Pythia (P.) 
scarabaeus (Linnaeus), radula; B, Pythia (P.) scarabaeus, reproductive system; C, Pythia (P.) plicata (Fér- 
ussac), central nervous system; D, Pythia (P.) scarabaeus; E, Pythia (Trigonopythia) trígona (Troschel); F, 
Ophicardelus australis (Quoy & Gaimard); G, Myosotella myosotis (Draparnaud); H, Ovatella firminii Pay- 
raudeau; I, Laemodonta octanfracta (Jonas); J, Allochroa bronni (Philippi); K, Cassidula (C.) aunsfelis (Bru- 
guière); L, Cassidula (Cassidulta) doliolum (Petit); M, Cylindrotis quadrasi Möllendorff; N, Aurículastra subula 
(Quoy & Gaimard); O, Ellobium (E.) aurísmidae (Linnaeus), radula; P, Ellobium (E.) aunsmidae, reproductive 
system; Q, Ellobium (E.) aurísmidae, central nervous system; R, Ellobium (E.) aurísmidae; S, Ellobium 
(Aurículodes) gangeticum (Pfeiffer); Т, Aurículinella (Leucophytia) bidentata (Montagu); U, Blaunería hetero- 
clita (Montagu); V, Carychium trídentatum (Risso), radula; W, Carychium trídentatum, reproductive system; 
X, Carychium trídentatum, central nervous system; Y, Carychium minimum Müller; Z, Zospeum spelaeum 
(Rossmässler); AA, Pedipes mirabilis (Mühlfeld), radula; BB, Pedipes pedipes (Bruguière), reproductive 
system; CG, Pedipes pedipes, central nervous system; DD, Pedipes pedipes; ЕЕ, Marínula pepita King; FF, 
Creedonia succinea (Pfeiffer); GG, Pseudomelampus exiguus (Lowe); HH, Sarnia frumentum (Petit); II, 
Microtralia occidentalis (Pfeiffer); JJ, Leuconopsis obsoleta (Hutton); КК, Melampus (M.) coffeus (Linnaeus), 
radula; LL, Melampus (M.) coffeus, reproductive system; MM, Melampus (M.) coffeus, central nervous 
system; NN, Melampus (M.) coffeus; 00, Melampus (Micromelampus) nucleolus Martens; PP, Melampus 
(Detracia) bullaoides (Montagu); QQ, Melampus (Signia) granifer (Mousson); RR, Tralla (T.) ovula (Bruguière); 
SS, Tralia (Persa) costata (Quoy & Gaimard). 



conopsis Hutton, and have created the genus 
Creedonia. Myosotella Monterosato, treated 
by Zilch as a subgenus of Ovatella Bivona, is 
given herein generic status. 

A pictorial review of the subfamilies is pre- 
sented In Figure 3. The radula, nervous sys- 
tem and reproductive system of the type or of 
a representative species of each subfamily 
are shown, as well as the shells of all the type 
species of the genera and subgenera herein 
recognized. The reproductive and nervous 
systems provided the most consistent basis 
for the separation of the subfamilies. 



Detailed descriptions of general anatomy 
and of the nervous system are provided un- 
der Melampus (M.) coffeus; these descrip- 
tions will be used as standards of compari- 
son in discussions of other species. 

Habitat: Ellobiids are mainly tropical. They 
commonly occur around the high-tide mark in 
mangrove areas, under rocks or pieces of de- 
caying wood. In extratropical regions they live 
in eurhyaline environments of salt marshes or 
in upper littoral rocky areas. 
Morton (1955c) divided the ellobiids into 



176 



MARTINS 



four groups according to habitat. The upper- 
tidal marine ellobiids, such as Melampus, 
Myosotella, Ophicardelus, Cassidula and El- 
lobium, prefer the high-tidal fringe of man- 
groves and marshes, never venturing far from 
the reach of the highest spring tides. The in- 
tertidal and crevice-dwelling species include 
the minute ellobiids of the genera Auricu- 
linella, Leuconopsis, Pedipes, Microtralia and 
Marinula, to which Creedonia, Laemodonta 
and Blauneria might be added, which live 
buried at different depths in the sediment or 
under partly buried rocks, roots and fallen 
branches in the upper intertidal zone. Pythia 
is the only coastal terrestrial ellobiid; it always 
frequents moist places near the shore, al- 
though out of reach of the highest tides. The 
inland terrestrial ellobiids are Carychium and 
Zospeum, which live in very humid environ- 
ments, frequently under forest leaf litter or in 
caves. 

The ellobiids are commonly thought to have 
evolved from an estuarine ancestor. Con- 
quest of the terrestrial habitat brought about 
modifications in the structure of the larval 
stages. Such modifications, however, are not 
exclusively related to distance from the sea 
and a single feature, such as suppression of 
a free-swimming veliger, can exist in intertidal 
and terrestrial species. A more or less mod- 
ified veliger stage is present throughout the 
family. The Melampinae have a free-swim- 
ming veliger larva. Apley (1970) recorded two 
to six weeks of planktonic life for Melampus 
(M.) bidentatus, while Marcus & Marcus 
(1965a) suggested equally long periods for 
the veligers of Melampus (M.) coffeus and 
Melampus (D.) paranus. The veliger stage of 
the other subfamilies passes inside the egg 
and the embryo crawls immediately after 
hatching. Larvae of Ellobium (A.) dominicense 
have a ciliate velum and can swim for very 
short periods of time (Ewald, 1963). That 
same ciliated structure was found in Blauneria 
heteroclita by Marcus & Marcus (1963). Mor- 
ton (1955c) observed that the velum of the 
larvae of Myosotella myosotis and of Auricu- 
linella (L.) bidentata is reduced and lacks cilia. 

Another feature of larval ellobiids is the 
widespread presence of an operculum, which 
is lost at an early age. Blauneria heteroclita, 
which normally reaches 7 mm in length, sheds 
the operculum at a shell length of about 0.7 
mm (Marcus & Marcus, 1963). The reduced 
operculum of Myosotella myosotis and of Ли- 
riculinella (L) bidentata helps to break the 
shell during hatching (Morton 1955b). 



Range: The family Ellobiidae has worldwide 
distribution, but appears to have three main 
centers, a large Indo-Pacific center, charac- 
terized by Ellobium, Cassidula and Pythia; a 
smaller West Indian center, characterized by 
Melampus; and a much poorer Mediterra- 
nean region, characterized by Myosotella and 
Ovatella. 

The fossil record of the Ellobiidae is rela- 
tively poor and is insufficient for the determi- 
nation of evolutionary lineages. The presence 
of the Indo-Pacific genera Ellobium and Cas- 
sidula in Europe during the Eocene and 
Miocene (Zilch, 1959) suggests that the Eu- 
ropean shores were connected with the Indo- 
Pacific region. This is consistent with the ex- 
istence of the Tethys Sea which, in various 
ways, extended longitudinally from Australia 
through Europe and northern Africa to the 
tropical West Indies and eastern Pacific. 
Existence of this seaway is indicated by the 
distribution of several groups of inverte- 
brates, and has been more extensively stud- 
ied for the Mediterranean region. Evidence 
of a Tethyan distribution in American faunas 
was found in Foraminifera (CG. Adams, 
1967), Ostracoda (McKenzie, 1967) and in bi- 
valves and gastropods (Palmer, 1967). The 
ellobiid fossil record does not provide any 
new information about Tethyan relationships 
between Europe and America. The ellobiid 
fossils of North America are represented by 
the melampinine genera Rhytophorus and 
Melampoides from the Cretaceous of Wyo- 
ming (White, 1895; Henderson, 1935) and by 
the more recent Melampus, Marinula, Tralia 
and Pedipes, from the Eocene, Miocene and 
Pleistocene (Conrad, 1 862; Dall, 1 91 2; Wood- 
ring, 1928; Gibson-Smith & Gibson-Smith, 
1979, 1982, 1985). The Mesozoic genera 
seem not to have European counterparts, 
but Rhytophorus was recorded from the 
Lower Cretaceous of China (Zhu, 1980). 
Present records are too sparse to allow elab- 
oration of the meaning of such an occur- 
rence. The Cenozoic genera represent only 
the Recent ellobiid fauna of the West Indian 
region. 



Subfamily Ellobiinae H. & A. Adams in Pfeif- 
fer, 1854 

Auriculea Pfeiffer, 1853a: 9. 

Ellobiinae "H. & A. Adams" Pfeiffer, 1854b: 
146. 

Auriculinae H. & A. Adams, 1855a; 30 [emen- 
dation of Auriculea Pfeiffer, 1853]. 



WESTERN ATLANTIC ELLOBIIDAE 



177 



Description: Shell very small and thin {Auri- 
culinella, Blauneha) to large and thick {Ello- 
bium), dextral except in Blauneha. Spire low 
to high, with very faint to marked and granu- 
lar spiral lines. Body whorl 60-80% of shell 
length, smooth or sculptured like spire. Ap- 
erture 70-80% of length of body whorl, oval- 
elongate; columellartooth small, very oblique; 
anterior parietal tooth stronger, perpendicular 
to (Auriculinella) or weakly oblique to columel- 
lar axis; smaller posterior parietal teeth some- 
times present; outer lip thin and sharp to thick 
and weakly reflected, smooth internally. Pro- 
toconch smooth, prominent, with umbilicus- 
like slit in apex. 

Radula with central tooth small, triangular; 
lateral teeth bicuspid, with endocone smaller 
than mesocone; marginal teeth similar to lat- 
eral teeth but smaller. 

Animal whitish; eyes often concealed by 
thick skin; tentacles short, subcylindric or 
with dilated tips; foot entire {Ellobium) or 
transversely divided. Mandible corneous, 
semilunate. Stomach tripartite; mid-section 
very muscular. Spermiduct separates from 
oviduct before the latter leaves posterior 
glandular complex; anterior mucous gland 
covers entire length of vagina; spermiduct 
surrounded by prostate gland and might 
communicate with base of bursa duct near 
vaginal opening. Penis large and complex to 
small and simple {Blauneha); associated vas 
deferens adheres to penis. Visceral nerve 
ring long, with evidence of streptoneury in 
Ellobium; right parietovisceral connective 
very short. 

Remarks: There has been confusion in defin- 
ing the limits of the subfamily Ellobiinae. 
Pfeiffer (1853a) was the first to try to group 
the genera of the Ellobiidae into higher taxa. 
On the basis of the absence or presence of a 
reflected outer lip he recognized the subfam- 
ilies Melampea and Auriculea. He assigned 
Pythia, Auhcula [= Ellobium] and Carychium 
to the latter group. The two subfamilial 
names were emended to Melampinae and 
Auhculinae by H. & A. Adams (1 855a). Pfeiffer 
(1854b), after seeing the unpublished manu- 
script of the Genera of Recent Mollusca by H. 
& A. Adams (1855), mentioned some of the 
Adams' conclusions, including the names 
Melampinae and Ellobiinae, and it is H. & A. 
Adams (in Pfeiffer) who should be credited 
with the introduction of the latter name (see 
the remarks under the Ellobiidae). Pfeiffer 
(1854b) continued to use his previous names 



and to the existing list of the Auriculea he 
added Plecotrema [= Laemodonta], Cassid- 
ula, Alexia [= l\Âyosotella] and Blauneha. Two 
years later in his Monografía Pfeiffer (1856a) 
tentatively included the genus Leuconia [= 
Auhculinella] in this subfamily. 

Odhner (1925) noted the peculiar radula of 
Ellobium and he admitted only this genus to 
the subfamily. He wrongly stated that Ello- 
bium (E.) auhsmldae lacks the central radular 
tooth (Fig. 17). Zilch (1959), who used con- 
chological characters, also considered the 
Ellobiinae monotypic. Thiele (1931), on the 
basis of radular morphology, reached quite 
different conclusions and he included in the 
Ellobiinae the subfamilies Melampinae, Pythi- 
inae and Cassidulinae. 

Studies of the comparative anatomy of the 
group are essential to an understanding of 
the taxonomic relationships within the Ellobi- 
inae and of the entire family as well. Morton 
(1 955c) noticed the similarity of the reproduc- 
tive tracts of Auhculinella and Ellobium, and 
placed those two genera in the subfamily El- 
lobiinae. Likewise on the basis of reproduc- 
tive structures Marcus (1965) and Marcus & 
Marcus (1965b) added Blauneha. In spite of 
the sinistrality of Blauneha and the fact that 
Blauneha and Auhculinella are much smaller 
than Ellobium, the dentition of the inner lip 
shows a constant pattern in all three genera 
of the subfamily. This conchological similar- 
ity, corroborating the evidence shown by the 
reproductive system, makes these features 
useful phylogenetic characters. I therefore 
concur with the inclusion of Auhculinella and 
Blauneha in the subfamily Ellobiinae. 

Habitat: The various genera of the Ellobiinae 
live in somewhat different habitats. Ellobium 
is common on the muddy surface of Indo- 
Pacific mangroves, just below the high-tide 
mark, around roots and decaying wood 
(Berry et al. 1967). Blauneha lives buried in 
the black sediment, and under rocks and rot- 
ting vegetable material at the high-tide mark 
(Marcus & Marcus 1965b; Martins, personal 
observation). Auhculinella lives closer to the 
low-tide mark than the other two genera; in 
the Azores it lives under rocks buried in 
gravel, sometimes into the intertidal zone 
(Martins, 1980). 

Range: The Ellobiinae have a worldwide dis- 
tribution, with only partial overlap of the dif- 
ferent genera. Ellobium, which is character- 
istic of the Indo-West Pacific mangroves, has 
a single representative in the tropical Eastern 



178 



MARTINS 



Pacific and another in the tropica! Western 
Atlantic. Blauneria occurs only in the Western 
Indo-Pacific and in the Western Atlantic. Au- 
riculinella is restricted to the Mediterranean, 
the eastern North Atlantic and Macaronesian 
Islands. 

The subfamily seems to have had a 
Tethyan distribution, which is shown by the 
present distribution of Ellobium and by the 
presence of Ellobium and the Blauneria-Wke 
StoHdoma Deshayes in the Jurassic and Oli- 
gocène deposits of Europe (Degrange- 
Touzin, 1893; Zilch, 1959; Huckriede, 1967). 

Genus Ellobium Röding, 1798 

Ellobium Röding, 1798: 105. Type species by 
subsequent designation of Gray (1847a): 
Ellobium midae Röding, 1798 [= Bulla 
aurismidae Linnaeus, 1758]. 

Auricula Lamarck, 1799: 76. Type species by 
monotypy: Auricula midae (Röding, 
1798) [= Bulla aurismidae Linnaeus, 
1758]. 

Auriculus Montfort, 1810: 310. Type species 
by monotypy: Auriculus judae Montfort, 
1 81 [= Bulla aurisjudae Linnaeus, 1 758]. 

Marsyas Oken, 1815: 305 [new name for El- 
lobium Röding]. 

Geovula Swainson, 1840: 344 [new name for 
Ellobium Röding]. 

Description: Shell moderately large and thin 
(25 mm) to large and thick (1 00 mm) and cov- 
ered with pale brown periostracum. Spire low 
to moderately high, sculptured with granular 
spiral lines crossed by more or less conspic- 
uous axial cords. Body whorl about 80% 
shell length, with same sculpture as spire, 
sometimes weakly depressed dorsoventrally. 
Aperture about 80% length of body whorl; 
small, very oblique, twisted columellar tooth; 
stronger anterior parietal tooth; posterior pa- 
rietal tooth sometimes present; outer lip thin 
to thick, sharp to weakly reflected. 

Radula with central tooth small, very nar- 
row, without mesocone, with ectocones 
curved inwards; lateral teeth with very wide, 
bicuspid crown; marginal teeth similar to lat- 
eral teeth, but smaller. 

Remarks: The name Ellobium Röding, 1798, 
was ignored for a long time in favor of its 
junior synonym Auricula Lamarck, 1799. 
Most probably the reason for maintaining the 
junior name was the acceptance of La- 
marck's work and ignorance of the Bolten 
Catalogue published by Röding in 1798 (Fis- 



cher, 1857; Dall, 1915). The vernacular name 
Auricule was first published by Lamarck in 
the Actes de la Société d'Histoire Naturelle 
de Paris in 1 795 or 1 796 [fide Férussac, 1 821 : 
95), but the Latinized name Auricula first ap- 
peared in Lamarck's (1799) Prodrome, pub- 
lished in the Mémoires of the same society. 

Montfort (1810) pointed out that Lamarck 
(1 799) had confused Auricula midae and Au- 
ricula judae by including in the references Ar- 
genville's (1 757: 226, pi. 1 [1 3], fig. G) "oreille 
de Midas," which Montfort identified with Ли- 
ricula judae. Montfort, then, renamed La- 
marck's genus Auriculus and selected for its 
type species Auriculus judae [= Ellobium (E.) 
aurisjudae (Linnaeus)]. Pfeiffer (1876) pre- 
ferred Auriculus Montfort to Ellobium Röding 
and Auricula Lamarck, both of which he dis- 
missed as vague, owing to the heterogeneous 
assemblage of species that they included. 

The genus Ellobium is conchologically well 
characterized by its auriform shape, by a 
finely reticulate sculpture and by the conspic- 
uous straw-colored to dark brown perio- 
stracum (Figs. 4-9). The central tooth of the 
radula is greatly reduced but not lost in Ello- 
bium (E.) aurismidae, as Odhner (192.5) erro- 
neously reported (Fig. 17). The mesocone of 
the central tooth has been lost and the ecto- 
cones curl inwards and resemble a pair of 
pincers (Figs. 13, 14). 

Zilch (1959), on the basis of conchological 
characters, recognized the subgenera Ello- 
bium s.S. and Auriculodes Strand. Ellobium 
was characterized as having a large, thick 
shell with a thick, reflected outer lip (Fig. 9), 
whereas Auriculodes had a smaller, thinner 
shell, with the outer lip sharp and weakly re- 
flected (Figs. 4-8). Some scattered informa- 
tion on the reproductive system of species 
belonging to both subgenera (see remarks 
under Auriculodes) indicates that the penis 
and vagina are usually more complex in Ello- 
bium s.S. More detailed research on a greater 
number of species of both subgenera is 
needed, however, to clarify the relative taxo- 
nomic positions of Ellobium s.s. and Auricu- 
lodes. Pending additional information, on the 
basis of shell thickness, I concur with Zilch 
(1959) in the recognition of these subgenera. 

Subgenus Auriculodes Strand, 1928 

Autonoe Guppy, 1868: 244. Type species by 
monotypy: Autonoe riparia Guppy, 1 868 
[= Auricula dominicense Férussac, 
1821]. Non Leach, 1852. 



WESTERN ATLANTIC ELLOBIIDAE 



179 



Auriculina Kobelt, 1 898: 77. Type species by 
original designation: Auricula (Auriculina) 
gangetica Pfeiffer, 1855. Non Grateloup, 
1838, nee Agassiz, 1847. 

Auriceila Möllendorff, 1898: 160. Type spe- 
cies by original designation: Auricula 
(Auriceila) auricella Férussac, 1821 [= 
Bulimus auricula Bruguière, 1789]. Non 
Jurine, 1817. 

Auriculodes Strand, 1928: 64 [new name for 
Auriculina Kobelt, 1898]. 

Autonoella Wenz, 1947: 36 [new name for 
Autonoe Guppy, 1868]. 

Description: Shell to 25 mm long, thin to 
somewhat solid. Spire with fine spiral lines, 
sometimes granular and crossed by axial 
granular cords. Body whorl not flattened dor- 
soventrally, smooth and shiny or with granular 
appearance as in spire. Inner lip of aperture 
with very oblique, twisted columellar tooth 
and somewhat stronger, weakly oblique pa- 
rietal tooth; outer lip sharp, sometimes slightly 
thick and somewhat sinuous at mid-length, 
slightly reflected in gerontic specimens. 

Animal with portion of vagina anterior to 
confluence with bursa duct straight, very 
short; associated vas deferens adhering to 
anterior vagina; penis moderately long, 
straight; associated vas deferens adhering to 
penis. 

Remarks: Guppy (1868), on the basis of a 
single beach specimen, introduced Autonoe 
[= Autonoella Wenz], which he considered al- 
lied to Melampus and Laimodonta [= Laem- 
odonta]. Later, in the revised list of the spe- 
cies of Trinidad, Guppy (1872: 7) observed 
under Synonyms, etc., "Comp. Auricula pel- 
lucens [= Ellobium (A.) dominicense (Férus- 
sac)]." Thiele (1931) considered Autonoe a 
subgenus of Melampus, as did Zilch (1959) 
for Autonoella Wenz, a replacement name for 
the preoccupied Autonoe Guppy. From the 
original description of Autonoella riparia 
(Guppy), and from Guppy's illustration (1871: 
pi. 1 7, fig. 1 ), it seems that the specimen con- 
sidered was a juvenile of Ellobium (A.) domin- 
icense (Férussac). In view of this, I consider 
Autonoella Wenz a junior synonym of Auric- 
ulodes Strand. 

Kobelt (1898) proposed Auriculina at the 
same time as Möllendorff (1898) introduced 
Auricella for the smaller and thinner-shelled 
forms of Ellobium s.l. Because both names 
were preoccupied. Strand (1928) introduced 
the substitute name Auriculodes for Kobelt's 
Auriculina. 



Only two species oi Auriculodes have been 
investigated anatomically, and they appar- 
ently differ greatly from each other in their 
palliai gonoducts. According to Marcus & 
Marcus (1965b) and Martins (this study) Ello- 
bium (A.) dominicense has a very short, 
straight vaginal section anterior to the con- 
fluence with the bursa duct, and a moder- 
ately long, straight penis. Knipper & Meyer 
(1956) briefly described the reproductive sys- 
tem of Ellobium (A.) gaziense (Preston, 1913) 
and they mentioned the lack of separation 
between male and female ducts. This feature 
is not typical of the subfamily and could lead 
to removal of Ellobium (A.) gaziense, a spe- 
cies with typical Auriculodes shell (Fig. 8), 
from the Ellobiinae. Knipper & Meyer's rep- 
resentation of the nervous system is so sim- 
ilar to that of Ellobium (A.) dominicense (Mar- 
tins, this paper), however, that the accuracy 
of their report on the reproductive system 
should be questioned instead. Apparently 
there are variations in the penial structure of 
Ellobium s.S. as well. The highly coiled penis 
of Ellobium (E.) aurisjudae (Linnaeus) is typi- 
cal of the nominate subgenus (Morton, 1 955b; 
Berry et a!., 1967). Sumikawa & Miura (1978) 
observed a thick, straight penis in Ellobium 
(E.) chínense (Pfeiffer) although this species 
retains the characteristic long, coiled anterior 
vagina. Odhner (1925: pi. 1, fig. 10), on the 
other hand, represented a small, somewhat 
thickened, straight penis, and an equally 
straight vagina for Ellobium (E.) subnodosum 
(Metcalfe, 1851). All of these scattered ana- 
tomical observations on the genus hardly al- 
low conclusions to be drawn concerning the 
correlation between conchological and ana- 
tomical characters of these two subgenera, 
but I find the conchological characters suffi- 
cient to justify the separation of Auriculodes 
from Ellobium s.s. 

Habitat: Species of the subgenus Auricu- 
lodes prefer to live above the high-tide mark 
of mangrove swamps, gathering wherever 
there is rotten wood (Morrison, 1946; Marcus 
& Marcus, 1965b; Keen, 1971; Martins, per- 
sonal observation). 

Range: The subgenus Auriculodes is known 
from the eastern coast of Africa (Knipper & 
Meyer, 1956) and throughout the Indo-Pa- 
cific region. It is represented along the west- 
ern coast of Central America by Ellobium (A.) 
stagnate (Orbigny, 1835) and in the West In- 
dian region to Brazil by the closely related 
Ellobium (A.) dominicense (Férussac). 



180 



MARTINS 



Ellobium (Auriculodes) dominicense 

(Férussac, 1821) 

Figs. 4-7, 10-16, 18-22 

Auricula dominicensis Férussac, 1821: 103 
[Santo Domingo Island (Hispaniola); lec- 
totype herein selected MNHNP (Fig. 4)]; 
Beck, 1837: 103; Beau, 1858: 15. 

Auricula pellucens Menke, 1828: 78 [Demer- 
ara (Guyana), South America; location of 
type unknown]; Menke, 1830: 36, 131; 
Küster, 1 844: 1 7, pi. 2, figs. 16,17; Pfeif- 
fer, 1854b: 151; Pfeiffer, 1856a: 137; Bin- 
ney & Bland, 1870: 87; Simpson, 1889: 
68. 

Conovulus pellucens (Menke). Voigt, 1834: 
111. 

Ellobium pellucens (Menke). H. & A. Adams, 
1855b: 237; Morrison, 1951b: 10; Perry 
& Schwengel, 1955: 197, pi. 39, fig. 185; 
Morrison, 1958: 123; Marcus, 1965: 
124-128 [taxonomy]; Marcus & Marcus, 
1965b: 426-438, pi. 1, figs. 1-7, pi. 2, 
figs. 8-11, pi. 3, figs. 12-16 [anatomy, 
ecology, taxonomy]; Rios, 1970: 139; 
Abbott, 1974: 334, fig. 4106 [illustration 
from Dall (1885)]; Rios, 1975: 159, pi. 48, 
fig. 769; Altena, 1975: 88; Vokes & 
Vokes, 1983: 60, pi. 22, fig. 18. 

Autonoe riparia Guppy, 1868: 244 [Mayaro 
Point, Trinidad; type presumed to be in 
Victoria Institute, Trinidad, destroyed by 
fire in 1920 (Sherborn, 1940); Guppy, 
1871: 306, pi. 17, fig. 1 [type figured]; 
Guppy, 1872: 7. 

Melampus riparius (Guppy). Pfeiffer, 1876: 
317. 

Auriculus pellucens (Menke). Pfeiffer, 1876: 
359. 

Auricula (Auriculastrum) pellucens Menke. 
Dall, 1885: 275, pi. 18, fig. 8; Dall, 1889: 
90, pi. 47, fig. 8; Maury, 1922: 54. 

Auhculastra pellucens (Menke). Kobelt, 1898: 
101, pi. 15, figs. 5, 6; Haas, 1950: 197; 
Ewald, 1963: 11-14 [larval history]. 

Melampus (Autonoe) riparius (Guppy). Ko- 
belt, 1898: 213, pi. 25, figs. 5, 6; Thiele, 
1931: 467. 

Auriculastrum pellucens (Menke). C.W. 
Johnson, 1934: 158; M. Smith, 1937, pi. 
67, fig. 8 [plate from Dall (1885)]; Webb, 
1942, pi. 11, fig. 21; M.Smith, 1951: 145, 
pi. 55, fig. 2, pi. 67, fig. 8; Coomans, 
1958: 103. 

Melampus (Autonoella) riparius (Guppy). 
Zilch, 1959: 66, fig. 210. 



Description: Shell (Figs. 4-7, 10, 11) to 27 
mm long, oval-elongate, somewhat solid, 
whitish-yellowish, covered with brownish pe- 
riostracum. Spire with as many as eight 
weakly convex whorls; sculpture as in sub- 
genus. Body whorl about 85% of shell length, 
subcylindric, smooth or with same sculpture 
as spire. Aperture about 80% length of body 
whorl. Inner partition of whorls occupying 
one-third of body whorl (Fig. 6). Protoconch 
smooth, prominent, with about one whorl vis- 
ible; lip weakly reflected at base, forming um- 
bilicus-like perforation in apex (Figs. 10, 11). 

Animal white; tentacles partly retractable, 
moderately long, subcylindhcal, with swollen 
tip; eyes inside base of tentacles, deep in 
integumentum, barely visible; foot entire; 
mantle skirt white; anal opening continued by 
fold of mantle skirt forming longitudinally split 
tubular extension. Kidney long, narrow, whit- 
ish. 

Radula (Figs. 13-16, 18) with formula 
(26+1+26)x70. Central tooth small; base 
roughly rhombic; posterior portion elongate, 
emarginate at anterior quarter, where crown 
of next tooth seems to articulate; crown very 
small; mesocone lacking; endocones thin, 
sometimes curled inwards. Lateral and mar- 
ginal teeth not sharply distinct, here de- 
scribed always as lateral teeth; first seven to 
12 with base short and wide, weakly pro- 
jected lateroanteriorly, with median anterior 
notch with which posterior process of crown 
of next tooth articulates; crown wide, roughly 
triangular, bicuspid, with conspicuous poste- 
rior process; mesocone wide, somewhat 
rounded anteriorly; endocone sometimes 
barely defined, mainly in adult specimens; 
gradual narrowing of crown and somewhat 
sharper definition of endocone marks teeth 
1 2 to 21 ; base shorter and narrower than that 
of first group of lateral teeth, with lateral pro- 
jection resembling basal ectocone; crown 
somewhat narrow, elongate; endocone first 
very rudimentary, then absent; no clearly de- 
fined ectocone. 

Digestive system with mandible solid, 
crescentic, with concave, sharp anterior 
edge and tapered ends (Fig. 12). Salivary 
glands fusiform, separated from each other, 
attaching to whitish esophagus by thin liga- 
ments. Stomach tripartite (Fig. 19); anterior 
portion membranous, comprising cardiac 
and pyloric regions; mid-portion (gizzard) 
very muscular, subcylindric; gastric caecum 
thin, receiving posterior diverticulum anteri- 



WESTERN ATLANTIC ELLOBIIDAE 



181 




FIGS. 4-1 1 . Ellobium. (4) E. (A.) dominicense (Férussac), lectotype (MNHNP), Santo Domingo [Hispaniola], 
s! 16.2 mm. (5) E. (A.) dominicense, Demerara, Guyana (ANSP 22251), s! 22.3 mm. (6) E. (A.) dominicense, 
Big Torch Key, Florida, si 20.6 mm. (7) E. (A.) dominicense, Big Torch Key, Florida, si 23.0 mm. (8) E. (A.) 
gaziense (Preston), syntype (BMNH 1969103), Gazi, British East Africa [Kenya], si 18.2 mm. (9) E. (E.) 
aurismidae (Linnaeus), Malaysia, si 90.4 mm. (10) E. (A.) dominicense, lateral view of spire and protoconch, 
Big Torch Key, Florida. (1 1) E. (A.) dominicense, top view of spire and protoconch. Big Torch Key, Florida. 
Scale 1 mm. 



orly. Digestive gland bilobed, brownish; pos- 
terior lobe conic, parlly covering ovotestis. 

Reproductive system (Fig. 20) with ovotes- 
tis follicular, covering posterior portion of 
stomach, beneath posterior lobe of digestive 
gland; hermaphroditic duct thin, straight; 
separation of male and female ducts just an- 



terior to fertilization chamber; secondary 
connection of posterior vas deferens with an- 
terior end of bursa duct; bursa duct as long 
as palliai gonoducts, emptying into oviduct a 
shorl distance from female aperture; anterior 
mucous gland covers oviduct as far as con- 
fluence with bursa duct. Penis moderately 



182 



MARTINÍ 




FIGS. 12-17. Ellobium, mandible and radular teeth. (12) E. (A.) dominicense, mandible, Big Torch Key, 
Florida; scale 1 mm. (13) E. (A.) dominicense, radula of young specimen, Big Torch Key, Florida, si 5.4 mm; 
scale 100 цт. (14) E. (A.) dominicense, radula of young specimen. Big Torch Key, Florida, si 5.4 mm; scale 
100 |im. (15) E. (A.) dominicense, radula of young specimen. Big Torch Key, Florida, si 5.4 mm; scale 200 
|im. (16) E (A.) dominicense, radula of young specimen, Big Torch Key, Florida, si 5.4 mm; scale 200 цт. 
(17) E. (E.) aurismidae, radula, Malaysia, si 90.4 mm; scale 200 |.im. 



long, somewhat thin, simple; ramifications of 
right tentacular retractor muscle attach to pe- 
nis near male aperture; associated vas defe- 
rens adhering to penis; penial retractor short, 
attaching to nuchal region. 
Nervous system (Fig. 21) with ganglia 



wrapped in thick connective tissue; cerebral 
commissure twice length of cerebral gan- 
glion; pedal commissure very short; left ce- 
rebropedal and cerebropleural connectives 
somewhat longer than right ones, about as 
long as cerebral commissure; pleuroparietal 



WESTERN ATLANTIC ELLOBIIDAE 



183 



с IL 2L 7L 8L 




9L lOL 11L 12L 17L 20L 24L 




FIG. 18. Ellobium (A.) dominicense, radula, Big 
Torch Key, Florida. Scale 10 цт. 




FIG. 19. Ellobium (A.) dominicense, stomach, Big 
Torch Key, Florida. Scale 1 mm. 



connectives very long; left parietovisceral 
connective shorter than right one, beneath 
branch of columellar muscle coming from be- 
hind right tentacle; right parietovisceral con- 
nective crossing over left one before insertion 
in visceral ganglion (rudiment of chiasto- 
neury); cerebral ganglia as large as pedal 
ganglia; left parietal ganglion double; anterior 
portion of left parietal ganglion giving off 
nerve to artery in mantle skirt, posterior por- 




FIG. 20. Ellobium (A.) dominicense, reproductive 
system. Big Torch Key, Florida. Scale 1 mm. 



tion giving off palliai internal and parietal cu- 
taneous nerves; osphradial ganglion present 
on pneumostomal nerve; tentacular nerves 
split at their origin; penial nerve coming off 
median lip nerve. 

Remarks: Ellobiuiv (A.) dominicense (Férus- 
sac, 1821) has been considered a synonym 
of Ellobium (A.) pellucens (Menke, 1828) al- 
though Dall (1885: 276) stated that Férus- 
sac's species was described in such a way 
as to be unidentifiable. Férussac's reference 
(1821: 103) to the sculpture and size of the 
shell and comparison with Auricula auricella, 
which he had just introduced, constitute 
enough indication to recognize the species. 
Contention might arise owing to the fact that 
Férussac's Auricula auricella was not de- 
scribed (Pfeiffer, 1856a: 134, footnote), but 
the author referred to Bulimus auricula Bru- 
guière, 1789, Lister (1770: pi. 577, fig. 326) 
[error for 32b] and Gualtieh (1742: pi. 55, fig. 
F). Férussac's description contains enough 
information to allow identification of the spe- 
cies and his name has priority over that of 
Menke (1828). 

Emerson & Jacobson (1976) considered 
Ellobium auricula (Bruguière) to be the earli- 
est name for the West Indian Ellobium. Bru- 
guière (1 789: 342) provided a description of a 
Bulimus auricula that indeed could apply to 



184 

gn cmn prcn 

\ vg ; ¡pan 

\ '. \ prvc ; ,' prg2 / 





MARTINS 










man 


pipe 


epic 


nn 


on 


ain 


prg1 


pc \ pcpn 


\ 


', 




,'cbc 



pcvn 



\W\ /// ^( 



piprc pmpn \ ^'\ alpn \ eg min 



'poen 




an 



prg ; ; 

I I 

mpan i 

pnn epari 



aepn 
eg pnn epan si ampri pen ptn 

FIG. 21. Ellobium (A.) dominicense, central nervous system, Big Torch Key, Florida. Scale 1 mm. 



ppn1 
pipn 

St 



I /'' /' pig / ; epc /'' / y 
în / aepri .' pin / trt 



pin / 
pen 



aoen 



the West Indian shells. No locality was given 
in the original description, and reference was 
made to the Gualtieri and Lister illustrations 
just cited. Férussac, as stated above, intro- 
duced without description Auricula auricella 
from Bale des Chiens Marins, New Cale- 
donia. He mentioned in his synonymy of Bru- 
guière's name the same synonymic refer- 
ences given by that author. The fact that 
some Indo-Pacific species are conchologi- 
cally very similar to the West Indian species 
contributed to this confusion. Ellobium (A.) 
dominicense has been stated erroneously to 
live in Natal, East Africa (Krauss, 1848), prob- 
ably the result of a misidentification of Ello- 
bium (A.) gaziense (Preston, 1913), and 
Pfeiffer (1856a) considered the Indian Ello- 
bium ceylanicum H. & A. Adams, 1 854, a jun- 
ior synonym of Auricula pellucens Menke, 
1828 [= Ellobium (A.) dominicense (Férussac, 
1821)]. All this circumstantial evidence indi- 
cates that Bruguière (1789) had described an 
Indo-Pacific shell, which was deposited at 
the Muséum d'Histoire Naturelle de Genève 
(Mermod & Binder, 1963). I therefore dis- 
agree with Emerson & Jacobson (1976), who 
misidentified Bruguière's name for the West 
Indian species. 
Ellobium (A.) dominicense has been placed 



wrongly in Auriculastra [Auriculastrum is an 
unjustified emendation (Marcus & Marcus, 
1965b)] by Dall (1885) and others. Martens 
(1880) created Auriculastra as a subgenus of 
Marinula for those species similar to Ellobium 
s.S., but with visible eyes and knobbed ten- 
tacle tips. Ellobium (A.) dominicense has 
these characteristics, a fact which might ex- 
plain Dall's decision. However, Auriculastra 
elongata (Parreyss, 1845), also originally 
listed by Martens and very similar to the type 
species, Auriculastra subula (Quoy & Gaim- 
ard, 1832), has a very different radula (Odh- 
ner, 1925) and appears to belong in the 
Pythiinae. 

The nervous system and the radula of the 
specimens of Ellobium (A.) dominicense here 
examined, collected on Big Torch Key, Flor- 
ida, differ from those of animals from Brazil 
studied by Marcus & Marcus (1965b). The 
central nervous system of the Floridian spec- 
imens is very similar to that of Ellobium (A.) 
gaziense (Preston), illustrated by Knipper & 
Meyer (1 956: 1 06, fig. 6), differing only in that 
the left parietal ganglion is double in Ellobium 
(A.) dominicense. In the Brazilian specimens 
(Marcus & Marcus, 1965b: 431, pi. 3, fig. 13) 
there is only one left parietal ganglion. The 
latter authors did not refer to the osphradial 



WESTERN ATLANTIC ELLOBIIDAE 



185 



ganglion and their figures indicate that the 
pleuroparietal connectives are shorter than 
the cerebropleural connectives. In the Florid- 
ian specimens the pleuroparietal connectives 
are three times longer than the cerebropleu- 
ral connectives. The radula of the specimens 
from Florida is very similar to those of Ello- 
bium (E.) auhsmidae (Fig. 17) and Ellobium 
(E.) aurisjudae, both from Malaysia. Marcus & 
Marcus (1965b: 433, pi. 2, fig. 8) described 
and figured a tricuspid central tooth with a 
small, triangular mesocone and rudimentary 
ectocones. In the specimens from Florida the 
mesocone is lacking and the slender ecto- 
cones are sometimes curved inwards, re- 
sembling small fangs. Preserved material 
from northern South America was not avail- 
able for comparative anatomical study; how- 
ever, intrapopulational variability in shell 
shape and intensity of sculpture is seen 
throughout the range of the species, al- 
though the sculpture seems to be more 
marked in northern South American speci- 
mens (Fig. 5). I am unsure about the phylo- 
genetic significance of the anatomical differ- 
ences observed in the Brazilian specimens. 
Should further comparative anatomical re- 
search establish that the South American 
specimens are a separate taxon, Menke's 
name pellucens is available. 

Deposited in the Muséum National d'His- 
toire Naturelle de Paris are two syntypes of 
Auricula dominlcensis Férussac, from which 
a lectotype is herein selected and figured 
(Fig. 4). 

Habitat: Ellobium (A.) domlnlcense lives in 
protected embayments in which mangrove 
growth is thin, buried in the soft black humic 
sediment or under rotting logs seldom cov- 
ered by high tide. It seems to be an oppor- 
tunistic species, usually found in colonies 
and apparently with very limited movement 
once established. Great numbers of shells 
clustered in a small area, indicative of former 
colonies, are often found without living ani- 
mals in the immediate vicinity. It seems that 
the colonies are destroyed by lack of food or 
by some environmental change, even though 
apparently suitable habitats exist a few 
meters away (Ewald, 1963; Marcus & Mar- 
cus, 1965b; Martins, personal observation). 

Range: Florida, from Miami to Cedar Key 
(Dall, 1885); Dominican Republic (Férussac, 
1821); Haiti; Guadeloupe (Beau, 1858); Trin- 
idad (Guppy, 1868); Yucatán, Mexico, to 




FIG. 22. Ellobium (A.) domlnlcense, geographic 
distribution. Open circle, locality from literature. 



Cananeia, Brazil (Marcus & Marcus, 1965b). 
(Fig. 22). 

Specimens Examined: FLORIDA: Golden 
Beach (MCZ 157854); Miami (ANSP 77056; 
MCZ 104943); Virginia Key (USNM 338303); 
Key Biscayne (ANSP 34521 0; USNM 700836, 
700911); Coconut Grove (MCZ 201646); El- 
liot Key (MCZ 110206); Key Largo (ANSP 
192837; MCZ 243979; USNM 590644, 
701 421); Card Sound, Key Largo (A.M.); Rab- 
bit Key (ANSP 88136); Big Pine Key (ANSP 
106384); Big Torch Key (USNM 61046, 
492482, 492484; A.M.); Middle Torch Key 
(USNM 663960); Oyster Bay (USNM 37596); 
Lossman Key (MCZ 291093); Cape Sable 
(MCZ 291 085, 292564; USNM 5251 56); Rog- 
ers River (MCZ 3981); 2.5 km E of Chokolos- 
kee Key (MCZ 58955); Harris Island, Ten 
Thousand Islands (USNM 381326); Blue Hill 
Island, near Goodland Point (ANSP 82742); S 
of Cape Romano (ANSP 62833); Marco (MCZ 
292565); Bonita Springs (MCZ 291088); Carl 
E. Johnson Park, near Little Carlos Pass 
(A.M.); Fort Myers (ANSP 66963, 140799; 
USNM 87733, 492483); Punta Passa (MCZ 
291091, 291094, 292566; USNM 39804); 
Punta Gorda (USNM 592297); Sanibel Island 
(ANSP 170650; MCZ 13721, 291089, 



186 



MARTINS 



291090, 292563); Bokeelia (MCZ 291087); 
Wulfen (ANSP 219866). HAITI: île-à-Vache 
(USNM 403877, 404948). MEXICO: Silam, 
Yucatán (ANSP 62656). VENEZUELA: N of 
Sinamaica, Zulla (USNM 536129). GUYANA: 
Demerara (ANSP 2225, 22241; MCZ 146522; 
USNM 31572, 58857, 119552). FRENCH 
GUIANA: Cayenne (MCZ 102934; USNM 
126413). SURINAME: Saramacca (USNM 
635276). 

Genus Blauneria Shuttleworth, 1854 

Blauneria Shuttleworth, 1854a: 148. Type 
species by monotypy: Blauneria cuben- 
sis (Pfeiffer, 1841) [= Voluta heterociita 
Montagu, 1808]. 

Blanneria Shuttleworth. Dali, 1885: 287 [in 
synonymy; error for Blauneria]. 

Blaumeria Shuttleworth. Verrill, 1901: 35 [er- 
ror for Blauneria]. 

Description: Shell to 8 mm long, elongate, 
fragile, translucent, whitish, sinistral. Spire 
with as many as nine flattened whorls. Body 
whorl about 60% of shell length. Umbilicus 
absent. Aperture about 70% of length of body 
whorl, oval-elongate; inner lip with very small 
columellar tooth; outer lip sharp, smooth. Pro- 
toconch prominent, smooth, with about one 
and one-half whorls visible. 

Radula having central tooth with wide, tri- 
angular, emarginate base; crown small, uni- 
cuspid. Lateral teeth gradually becoming 
smaller toward margin of radula, bicuspid, 
with strong mesocone and much smaller en- 
docone; no morphological distinction be- 
tween lateral teeth and marginal teeth. 

Animal whitish, translucent, with short, 
cylindrical tentacles and very conspicuous 
black eyes. Foot transversely divided. Ar- 
rangement of organs sinistral. Separation of 
male and female ducts just anterior to fertili- 
zation chamber, before oviduct enters pos- 
terior glandular complex; posterior vas defe- 
rens secondarily communicates with anterior 
end of bursa duct. Penis small, simple; asso- 
ciated vas deferens adhering to penis. Con- 
nectives of visceral nerve ring long. 

Remarks: The genus Blauneria is readily 
identifiable because it is the only sinistral el- 
lobiid taxon. The history of this once enig- 
matic small group, before it was placed tim- 
idly in a separate genus by Shuttleworth 
(1854a), is connected with that of the type 
species Blauneria heterociita (Montagu), and 



will be discussed in the remarks under that 
species. 

Once it was discovered to be a member of 
the Ellobiidae, the genus Blauneria was 
placed in different subfamilies, depending 
upon which character assumed greater im- 
portance in the classification scheme of the 
particular malacologist. Fischer & Crosse 
(1880) included Blauneria and other "marine" 
ellobiids with an elongated spire in the Auri- 
culinae [= Ellobiinae]. Odhner (1925), on the 
basis of radular characters, considered the 
genus to belong to the Cassidulinae. Thiele 
(1931), who based his classification largely 
upon Odhner's radular studies, did not rec- 
ognize the subfamilies Pythiinae and Cassid- 
ulinae, and placed Blauneria, together with 
many other genera, in the heterogeneous 
subfamily Ellobiinae. Zilch (1959), probably 
on the basis of conchological similarities with 
the dextral Cylindrotis Mollendorff, 1895, re- 
moved Blauneria to the Pythiinae. Finally, 
Marcus (1 965) and Marcus & Marcus (1 965b), 
followed by Hubendick (1978), included 
Blauneria in the Ellobiinae owing to similari- 
ties of the reproductive system with those of 
Ellobium and Auricullnella. My anatomical 
studies confirm the taxonomic conclusions of 
these latter authors. 

¡Habitat: Blauneria commonly lives in man- 
groves at the high-tide mark in the sediment 
under rocks and decaying branches. Pease 
(1869: 60) reported that his Blauneria gracilis 
from Hawaii lives in the same habitat as Pe- 
dipes, in the crevices of stones covered at 
high tide. He observed that Blauneria never 
crawls on the sides or tops of the rocks dur- 
ing low tide, but only around the base, which 
was always wet. 

Range: The genus is known from the warm 
regions of the Indo-Pacific and from the trop- 
ical Western Atlantic. There is no known fossil 
record of this sinistral genus, but the concho- 
logically closely related, dextral Stolidoma 
Deshayes, 1863, has been recorded from 
strata as old as the Paleocene of Europe (De- 
grange-Touzin, 1893; Zilch, 1959). Zhu (1980) 
described a Blauneria ? elliptiformis from the 
Cretaceous of northeastern China. 

Blauneria heterociita (Montagu, 1808) 
Figs. 23-40 

Voluta heterociita Montagu, 1808: 169 [Dun- 
bar, Scotland (error), herein corrected to 
Matanzas, Cuba; location of type un- 



WESTERN ATLANTIC ELLOBIIDAE 



187 



known]; Laskey, 1811: 398, pi. 81, figs. 
1, 2; Turton, 1819: 254. 

Acteon heteoclita (Montagu). Fleming, 1828: 
337. 

Achatina (?) pellucida Pfeiffer, 1840: 252 
[Cuba; location of type unknown]. 

Tornatellina cubensis Pfeiffer, 1841: 130 
[Cuba; location of type unknown]. 

Auricula lieteroclita (Montagu). Thorpe, 1844: 
146. 

Tornatella lieteroclita (Montagu). Forbes & 
Hanley, 1852: 526. 

Blauneria cubensis (Pfeiffer). Shuttleworth, 
1854a: 148; Franc, 1968: 525. 

Blauneria pellucida (Pfeiffer). Pfeiffer, 1854b: 
1 52; Pfeiffer, 1 856a: 1 53; H. & A. Adams, 
1858: 643, pi. 138, fig. 8; Binney, 1859: 
1 75, pi. 53, fig. 2; Binney, 1 860: 4; Binney, 
1865: 21, text fig. 22; Mörch, 1878: 5. 

Oleacina (Stobilus) cubensis (Pfeiffer). H. & A. 
Adams, 1855a: 136. 

Odostomla (Tornatellina) cubensis (Pfeiffer). 
Shuttleworth, 1858: 73. 

? Odostomla cubensis (Pfeiffer). Poey, 1866: 
394. 

Blauneria heteroclita (Montagu). Pfeiffer, 1 876: 
368; Arango y Molina, 1880: 60; Fischer 
& Crosse, 1880: 9, pi. 34, figs. 14, 14a 
14b [anatomy, radula, taxonomy]; Dall 
1885: 287, pi. 17, fig. 6; Dall, 1889: 92 
pi. 47, fig. 14; Simpson, 1889: 60 
Crosse, 1890: 259; Kobelt, 1900: 260, pi 
31, figs. 19, 20; Dall & Simpson, 1901 
369; Davis, 1904: 126; Peile, 1926: 88 
Thiele, 1931: 466; Bequaert & Clench 
1933: 538; C.W. Johnson, 1934: 160; M 
Smith, 1937: 147, pi. 67, fig. 14 [plate 
from Dall (1885)]; Morrison, 1951b: 10; 
Coomans, 1958: 104; Nowell-Usticke, 
1959: 88; Zilch, 1959: 74, fig. 241; 
Warmke & Abbott, 1961: 152; Marcus, 
1965: 124-128 [taxonomy]; Marcus & 
Marcus, 1965b: 438-446, pi. 4, figs 
25-29 [anatomy, taxonomy, habitat] 
Rios, 1970: 139; Abbott, 1974: 334, fig 
4104 [illustration from Binney (1859)] 
Altena, 1975: 87, fig. 42; Rios, 1975: 159 
pi. 48, fig. 768; Hubendick, 1978; 20, fig 
164, 24, fig. 176 [nervous and reproduc- 
tive systems redrawn from Marcus & 
Marcus (1965b)]; Vokes & Vokes, 1983: 
60, pi. 31, fig. 19; Jensen & Clark, 1986: 
458, pi. 153. 

Blanneria pellucida (Pfeiffer). Dall, 1885: 287 
[error for Blauneria; in synonymy]. 

Blaumeria heteroclita (Montagu). Verrill, 
1901: 35 [error for Blauneria]. 



Description: Shell (Figs. 23-32) with length 
to 7 mm, elongate, fragile, transparent to 
translucent, shiny, whitish. Spire with as 
many as nine flat or weakly convex whorls; 
very faint spiral lines on teleoconch, crossed 
by irregular growth lines. Body whorl about 
60% shell length in gerontic specimens, 70- 
75% in young individuals. Aperture about 
70% body whorl length, oval-elongate; inner 
lip weakly canaliculate at base, with small, 
very oblique columellar tooth, stronger, ob- 
lique parietal tooth at mid-length of aperture; 
outer lip sharp, smooth inside. Partition of 
inner whorls occupying about three-quarters 
of the body whorl (Fig. 26). Protoconch 
smooth, well developed, with one and one- 
half whorls visible, leaving umbilicus-like per- 
foration on apex (Figs. 30-32). 

Radula (Figs. 33-36) having formula (17 + 1 
+ 17) X 70. Base of central tooth wide, tri- 
angular, deeply emarginate anteriorly; crown 
very small, narrow, unicuspid. Lateral teeth 1 5 
to 18; base quadrangular, anteriorly oblique 
away from central tooth, with small notch on 
anterior edge; crown wider and longer than 
base, bicuspid; mesocone strong, long; en- 
docone less than half the length of mesocone; 
from about sixth lateral tooth outward a pro- 
cess develops on posterolateral edge of 
crown, which articulates with notch in base of 
next tooth. Marginal teeth not morphologi- 
cally distinct from lateral teeth except in grad- 
ual decrease in size. 

Animal has external anatomy as in genus. 
Stomach (Fig. 37) with thin, somewhat di- 
lated cardiac region, and smaller, slightly 
thicker pyloric region; gizzard very muscular, 
barrel-shaped; gastric caecum invaginable, 
without posterior diverticulum. 

Reproductive system (Fig. 38) with ovotes- 
tis apical, granular, orange; hermaphroditic 
duct simple, with some pouch-like dilations 
(seminal vesicle) as it approaches albumen 
gland; male and female ducts separating just 
anterior to fertilization chamber; spermiduct 
thick, covered with prostatic tissue, commu- 
nicating with bursa duct where the latter 
opens into vagina; anterior mucous gland 
covers oviduct until confluence with bursa 
duct. Penis small, simple; associated vas 
deferens adhering to penis; penial retractor 
very short, attaching to nuchal region. 

Nervous system (Fig. 39) with cerebral 
ganglia largest; cerebral commissure as long 
as width of cerebral ganglion; pedal commis- 
sure very short; right cerebropedal and cere- 
bropleural connectives longer than left coun- 



MARTINS 




FIGS. 23-35. Blauneria heterociita (Montagu). (23) Hungry Bay, Bermuda, si 6.7 mm. (24) Hungry Bay, 
Bermuda, si 5.2 mm. (25) Hungry Bay, Bermuda, si 4.3 mm. (26) Hungry Bay, Bermuda, si 6.3 mm. (27) 
Plantation Key, Flonda, si 3.5 mm. (28) Matanzas, Cuba (MCZ 131769), si 3.7 mm. (29) Isla Mujeres. 
Yucatán, Mexico (R.B.), si 3.5 mm. (30) Lateral view of spire and protoconch. Big Pine Key, Flonda. (31) Top 
view of spire and protoconch. Crawl Key, Florida. (32) Top view of spire and protoconch, West Summerland 
Key Flonda. (33) Lateral and central teeth of radula. Hungry Bay, Bermuda, si 4.5 mm. (34) Lateral and 
central teeth of radula, Hungry Bay, Bermuda, si 4.5 mm. (35) Lateral teeth of radula. Hungry Bay, Bermuda, 
si 4.5 mm. Scale, Figs. 30-32, 1 mm; Figs. 33-35, 100 |am. 



WESTERN ATLANTIC ELLOBIIDAE 

2L 3L 



189 




FIG. 36. Blauneha heterociita, radula, Hungry Bay, 
Bermuda. Scale 10 цт. 




FIG. 37. Blauneria heterociita, stomach, Hungry 
Bay, Bermuda. Scale 1 mm. 

terparts; left pleuropahetal and right parie- 
tovisceral connectives very long, the latter 
somewhat shorter than the former; right pleu- 
roparietal and left parietovisceral connectives 
about same size, about half length of cerebral 
commissure. 

Remarks: Blauneria heterociita (Montagu) 
was originally thought to belong to the En- 
glish malacofauna. The appearance of this 
Western Atlantic shell on the shores of Dun- 
bar, Scotland, can be attributed to the dump- 
ing of ballast of ships from the West Indies. 




FIG. 38. Blauneria heterociita, reproductive sys- 
tem. Hungry Bay, Bermuda. A-C, transverse sec- 
tions and their locations. Scale 1 mm. 



piprc pig pg pc cpc 




vg pfvc pipe 



FIG. 39. Blauneha heterociita, central nervous sys- 
tem. Hungry Bay, Bermuda. Scale 1 mm. 



This little, fragile and elegant shell puzzled 
the European naturalists for some time. 
Pfeiffer, within 12 months, introduced the 
names Achatina ? pellucida (1 840) and Tor- 
natellina cubensis (1841) for specimens from 
Cuba. H. & A. Adams (1855b, 1858) treated 
those two names as referring to species in 
very different groups. They assigned Torna- 
tellina cubensis to the terrestrial Oleacina, 
and they followed Pfeiffer (1854b) in allocat- 
ing Achatina ? pellucida to Blauneria. The 
species in question was placed in seven dif- 
ferent genera before Shuttleworth (1854a) 



190 



MARTINS 



hesitantly proposed that "Odostomia cuben- 
sis" probably should belong to a separate 
genus. Shuttleworth, in a presentation made 
at the Lyceum of New York a month before 
the appearance of that paper but published 
four years later, had considered the species 
to be marine on the word of the naturalist 
Blauner. Pfeiffer (1854b), upon receiving a 
communication from Gundlach that the ani- 
mal in question had conspicuous eyes at the 
base of the tentacles (Pfeiffer 1856a: 153), 
immediately adopted Shuttleworth's name 
Blauneria and placed the genus within the 
Auriculidae [= Ellobiidae]. 

I have found some discrepancies between 
the specimens I studied and those from Bra- 
zil examined by Marcus & Marcus (1965b). 
The Marcuses stated (p. 443) that the en- 
docone of the radular teeth is basal. The SEM 
photographs of my Bermudian specimens 
clearly show the endocone as part of the 
crown, not of the base (Figs. 33-35). Another 
discrepancy is found in the lengths of the 
pleuroparietal connectives of the visceral 
nerve ring (pi. 5, fig. 28). Based upon my ob- 
servations in the current study I suspect that 
the Marcuses reversed the right and left con- 
nectives. 

Blauneria differs from all other ellobiids in 
its sinistrality. Gerontic specimens have a 
very elongate and slender shell (Fig. 23). 
Most commonly, however, the body whorl of 
the shell is longer and wider than the spire 
(Figs. 27-29). This form has been the one 
commonly illustrated, represented by Binney 
(1865) and copied by Dall (1885), M. Smith 
(1937) and Abbott (1974). 

Habitat: Blauneria heteroclita lives in man- 
groves above the high-tide mark, where it is 
usually deeply buried in the soft sediment un- 
der rocks, rotten wood or on the roots of the 
propagules, where it occurs with Laemo- 
donta, Creedonia and Microtralla. Marcus & 
Marcus (1965b) stated that these animals are 
common in decaying banana trees washed 
ashore in Cananeia, Brazil. 

Range: Bermuda; Florida to Texas and Yu- 
catán, Mexico; West Indies; Panama (Olsson 
& McGinty, 1958); Suriname (Altena, 1975); 
Brazil (Flg. 40). 

Binney (1859: 176) stated, "Dr. Foreman 
collected a few specimens in a garden of 
Washington city. He believes them to have 
been brought on plants from Charleston, 
S.C." Both places are distant from the range 




FIG. 40. Blauneria heteroclita, geographic distribu- 
tion. Open circle, locality from literature. 

of the species and, because there has been 
no confirmation of either record, I do not in- 
clude them in the range of the species. 

Specimens Examined. BERMUDA: Fairyland 
(ANSP 99076); Old Road, Shelly Bay (A.M.); 
Cooper's Island (ANSP 131647); Hungry Bay, 
S of Ely's Harbour (both A.M.). FLORIDA 
(USNM 39843, 67953): St. Augustine (USNM 
663064); Rose Bay, N of New Smyrna Beach 
(A.M.); Miami (MCZ uncatalogued); Barnes 
Sound (ANSP 196748; MCZ 291100); Key 
Largo (MCZ uncatalogued; USNM 597460); 
Tavernier Key (USNM 492513); S of Ocean 
Dr., Plantation Key (A.M.); Lignumvitae Key 
(ANSP 156648; MCZ 294648); Lower Mate- 
cumbe Key (USNM 492521); Long Key 
(A.M.); Grassy Key (ANSP 397277; MCZ 
291102; A.M.); Crawl Key (A.M.); Big Pine 
Key (ANSP 1 041 06); end of Long Beach Drive 
and W of Kohen Avenue, both Big Pine Key 
(both A.M.); Sugarloaf Key (ANSP 88804, 
104107); Boca Chica Key (USNM 270352); 
Cape Sable (MCZ 291099, 291101); Marco 
(ANSP 22470; USNM 37615, 37616); Semi- 
nole Point (ANSP 105422); Starvation Key 
(ANSP 130061); Fort Myers (USNM 492512); 
E of St. James, Pine Island (ANSP 93432); 
Captiva Island (ANSP 149907); Sarasota Bay 
(USNM 30626); Mullet Key (USNM 652410, 



WESTERN ATLANTIC ELLOBIIDAE 



191 



653108; A.M.); Tampa Bay (USNM 37614); 
Boca Ciega Bay (ANSP 9570); Shell Key 
(USNM 466212); Clearwater Island (ANSP 
9350). AU\BAMA: Coden Beach (USNM 
422371). TEXAS: Galveston (MCZ 227843); 
Port la Vaca (MCZ 223050); N end of Padre 
Island, 45 km S of Port Aransas (MCZ 
228745). MEXICO: Isla Mujeres, Quintana 
Roo, Yucatán (R.B.). BAHAMA ISU\NDS: 
GRAND BAHAMA ISLAND: North Hawksbill 
Creek (ANSP 370564); South Hawksbill 
Creek (ANSP 371810); GREAT ABACO IS- 
LAND (ANSP 299496); ANDROS ISLAND: 
South Mastic Point (A.M.); Stafford Lake 
(ANSP 151931); Mangrove Key (USNM 
180672, 269947, 270198); Smith's Place, 
South Bight (USNM 257569, 269649); Under 
Key (USNM 270224); NEW PROVIDENCE IS- 
LAND: Nassau (MCZ uncatalogued); SE 
shore of Lake Cunningham (ANSP 299720); 
Bonefish Pond (A.M.); ROYAL ISU\ND 
(USNM 468124); AKLINS ISLAND: between 
Pleasant Point and Claret Cove (MCZ 
225524). CUBA (ANSP 22471; MCZ uncata- 
logued; USNM 39842, 57726, 492511): Ha- 
bana (ANSP 130745, 326340; MCZ 233993); 
Salt Works, Hicacos Peninsula (ANSP 
1 57338); La Chorrera (MCZ 1 28256, 1 67956); 
Cajio (MCZ 167955); Matanzas (MCZ 
131769; USNM 492510); Batabanó (ANSP 
93730; MCZ 167957). JAMAICA (ANSP 
16705, 22472; USNM 94765): Green Island 
Harbor (USNM 440791); Montego Bay (ANSP 
329122); Porl Morant (USNM 423688); King- 
ston (USNM 427130, 467555); Hunt's Bay 
(USNM 427117). HAITI: île-à-Vache (USNM 
403701, 403859, 403872, 404947); Landep- 
rie Bay (USNM 383264); between Vieux 
Bourg and Baïe des Flamands (USNM 
402467); Aquin (USNM 403149); Bizoton 
(USNM 403324). PUERTO RICO: Punta Are- 
nas, N of Joyuda (A.M.); Puerto Real (A.M.). 
VIRGIN ISLANDS: ST. THOMAS (ANSP 
22473). CARIBBEAN ISLANDS: GRAND 
CAYMAN ISLAND (ANSP 209768). BRAZIL: 
Cananeia (ANSP 305213; USNM 699448). 

Subfamily Pythiinae Odhner, 1925 

Scarabinae Fischer & Crosse, 1880: 5. 
Pythiinae Odhner, 1925: 14. 

Description: Shell variable in size. Aperture 
usually heavily dentate; one columellar tooth; 
one to three, commonly two parietal teeth, 
anterior one strongest; outer lip generally in- 
ternally dentate. 



Radula with mesocone of lateral teeth tri- 
angular, usually pointed; marginal teeth be- 
coming smaller toward margin, with as many 
as three subequal cusps. 

Animal with rudimentary anterior tentacles 
sometimes present; foot entire. Palliai gono- 
duct entirely hermaphroditic; anterior mu- 
cous gland and prostate gland covering 
spermoviduct along entire length; bursa duct 
emptying near vaginal opening; spermatic 
groove open in Pythia; penis simple; vas def- 
erens adhering to penis externally or free in 
haemocoel. Ganglionic connectives of vis- 
ceral nerve ring long, leaving pedal ganglia 
mid-way between cerebral ganglia and vis- 
ceral ganglion; right parietovisceral connec- 
tive longer than left one. 

Remarks: Fischer & Crosse (1880) created 
the subfamily Scarabinae for Scarabus Mont- 
fort, 1810 [= Pythia Röding, 1798] on account 
of its oddly shaped, dorsoventrally flattened 
shell. Odhner (1925) used the name Pythiinae 
because by that time Scarabus Montfort was 
recognized as a junior synonym of Pytliia 
Röding; he included Alexia [= Myosotella] and 
Blauneria on the basis of radular characters. 
Cassldula and Opiiicardelus were added by 
Morton (1955c), who merged Odhner's Cas- 
sidulinae with the Pythiinae. Zilch (1959) re- 
verted to Odhner's division and included in 
the Pythiinae the Recent genera Pythia, Ova- 
tella, Cylindrotis and Blauneria and removed 
Ophicardelus and Cassldula to the Cassiduli- 
nae. Marcus (1965) and Marcus & Marcus 
(1965b) noted that in Blauneria the spermi- 
duct and oviduct separate before the her- 
maphroditic duct enters the glandular com- 
plex, and so removed this genus to the 
Ellobiinae. In consideration of shell and ana- 
tomical features, I have concluded that Lae- 
modonta must be included in the Pythiinae. 

Dall (1885) included Sayella within the El- 
lobiidae and Zilch (1 959) listed it, with a ques- 
tion mark, within the Pythiinae. Morrison 
(1939), however, showed that Sayella Dall is 
not an ellobiid, but a pyramidellid opistho- 
branch. 

Separation of the Cassidulinae from the 
Pythiinae, as Odhner (1925) proposed and 
Zilch (1959) supported, is not justifiable. The 
two groups are similar in the basic pattern of 
the inner lip teeth of the shell aperture but 
their radular morphology shows too much di- 
versity and overlap to constitute a useful tax- 
onomic character at the subfamilial level. 
Both groups have a similar plan of the ner- 



192 



MARTINS 



vous system and, for this reason, Morton 
(1955c) regarded Odhner's Cassidulinae as 
superfluous. The nervous system of the Cas- 
sidulinae indeed shows the elongate right pa- 
rietovisceral connective, characteristic of the 
Pythiinae. Morton erroneously stated that the 
palliai gonoduct of Cassidula is very similar to 
that of Myosotella in that it remains hermaph- 
roditic until the vaginal aperture. According 
to Berry et al. (1967), Berry (1977) and Mar- 
tins (personal observation) the vas deferens 
of Cassidula aurisfelis (Bruguière) separates 
from the oviduct some distance before the 
vaginal opening, and runs free until entering 
the neck skin to follow the spermatic groove. 
This feature can be considered secondary to 
the general pattern of the reproductive sys- 
tem, however, for the bursa duct opens at the 
same position relative to the separation of 
the vas deferens in Cassidula as it does in the 
other Pythiinae. The same arrangement oc- 
curs in the Ellobiinae. Ellobium (E.) aurisjudae 
also has a long, nonglandular vagina, which 
is in accordance with the highly specialized 
penial complex of the species. Ellobium (E.) 
aurismidae, on the other hand, has a less 
specialized penis and lacks the long, non- 
glandular vagina (Morton, 1955c; Berry et al., 
1967; Martins, personal observation). In both 
species, however, the bursa duct opens at 
the anterior end of the glandular porlion of 
the oviduct. 

In view of the similarities of the repro- 
ductive and nervous systems of the two 
groups, as well as their similar patterns of 
apertural dentition, Morton's decision (1 955c) 
to merge the Cassidulinae with the Pythiinae 
is hereby followed. 

Habitat: The Pythiinae contain very primi- 
tive ellobiids such as Pythia, Myosotella, 
Ophicardelus and Cassidula. These groups 
have left the proximity of the sea and are less 
dependent upon that element than all other 
halophilic ellobiids. Pythia has acquired a 
semiterrestrial habitat, and Myosotella, Oph- 
icardelus and Cassidula were placed by 
Morton (1955c) among the "supratidal and 
estuarine ellobiids." Laemodonta lives in 
rocky areas at the high-tide mark, with Pe- 
dipes, and in the mangroves at or just below 
the high-tide mark, under rocks and fallen 
branches. 

Range: The Pythiinae have a worldwide 
distribution. Pythia, Cassidula and Ophicar- 
delus are characteristic of the tropical Indo- 



Pacific; Laemodonta, also common in the 
Indo-Pacific, is represented in the West Indies 
by one species. Ovatella and Myosotella are 
represented in the Mediterranean, but the 
latter has been introduced to eastern North 
America (Binney, 1859; Verrill, 1880), Califor- 
nia (Hanna, 1939), western South America, 
South Africa and Australia (Climo, 1982). 

Genus Mysotella Monterosato, 1906 

Phytia Röding, 1798. Gray, 1821: 231 [mis- 
spelling of Pythia]. 

Phitia Gray. Blainville, 1824: 246 [misspelling 
of Gray's misspelling of Pythia]. 

Phythya Gray. Deshayes, 1832: 762 [mis- 
spelling of Gray's misspelling of Pythia]. 

Jaminia Brown, 1827, pi. 51 . Type species by 
subsequent designation of Gray (1847a): 
Jaminia denticulata (Montagu, 1803) [ = 
Auricula myosotis Draparnaud, 1801]. 
Non Risso, 1826. 

Alexia "Leach" Gray, 1847a: 179. Type spe- 
cies by monotypy: Alexia denticulata 
(Montagu, 1803) [= Auricula myosotis 
Draparnaud, 1801]. Non Stephens, 
1835. 

Kochia Pallary, 1900: 239. Type species by 
subsequent designation of Monterosato 
(1906): Alexia (Kochia) oranica Pallary, 
1900 [= Auncula myosotis Draparnaud, 
1801]. Non Frech, 1891. 

Myosotella Monterosato, 1906: 126. Type 
species by original designation: Myoso- 
tella payraudeaui "Shuttleworth" Pfeif- 
fer, 1 856a [= Auricula myosotis Drapar- 
naud, 1801]. 

Nealexia Wenz, 1 920: 1 90 [new name for Al- 
exia Gray, 1847, non Stephens, 1835]. 

Deschption: Shell to 10 mm long, fragile to 
somewhat solid, pale yellow to purplish red. 
Spire high, with as many as eight weakly con- 
vex, spirally striated whorls; only one spiral 
row of hairs in juveniles. Aperture oval-elon- 
gate; inner lip with small, very oblique col- 
umellar tooth, strong anterior parietal tooth 
and usually one, sometimes more, parietal 
teeth becoming smaller posteriorly; outer lip 
sharp, weakly reflected, commonly with one 
or more inner tubercles. Protoconch smooth, 
large, with one and one-half protruding 
whorls, leaving umbilicus-like slit in apex of 
shell (Figs. 76, 77). 

Radula with base of central tooth wide, 
emarginate half of its length; crown of mar- 
ginal teeth pointing medially, mesocone 
stronger than endocone. 



WESTERN ATLANTIC ELLOBIIDAE 



193 



Animal grayish-white; neck and tentacles 
sometimes darkly pigmented. Hermaphro- 
ditic duct convolute; palliai gonoduct her- 
maphroditic as far as the vaginal aperture; 
anterior mucous gland and prostate gland 
cover entire length of spermoviduct; bursa 
duct emptying near vaginal aperture; penis 
short, thick; vas deferens adhering to penis. 
Ganglia of visceral nerve ring widely spaced; 
osphradial ganglion present. 

Remarks: The majority of modern literature 
has treated Myosotella Monterosato, 1906, 
as a subgenus of Ovatella Bivona, 1832. The 
anatomy of the type species of Myosotella, 
Myosotella myosotis (Draparnaud), has been 
studied extensively (Meyer, 1955; Morton, 
1955b) and Giusti (1973) looked briefly into 
the anatomy of the type species of Ovatella, 
Ovatella firminii (Payraudeau, 1826). A study 
of the anatomy of Ovatella aequalis (Lowe, 
1832) from the Azores (Martins, personal ob- 
servation) revealed the presence of a pallia! 
gland, not noted by Giusti (1973) for Ovatella 
firminii, similar to that in Carychium tridenta- 
tum (Müller) (Morton, 1955b), Pythia scara- 
beus (Gmelin, 1791) (Plate, 1897), Cassidula 
labrella (Deshayes, 1830) (Renault, 1966) and 
Laemodonta cubensis (Pfeiffer, 1854) (Mar- 
tins, this study). In another work (Martins, 
1980) Ovatella aequalis was shown to have 
a tripartite mandible with tapering ends, 
whereas that of Myosotella myosotis is entire 
and quadrangular. These two characteristics, 
corroborated by differences in the proto- 
conch, justify the attribution of generic rank 
to Myosotella. 

Some modern authors, following Kennard 
& Woodward (1919), treat Myosotella as a 
junior synonym of Gray's misspelling ^^Phy- 
tia" (Morrison, 1951a; M. Smith, 1951; Mc- 
Millan, 1968; Keen, 1971; Climo, 1982). The 
word "Phytia" appeared in Gray (1821) and is 
obviously a misspelling of Pythia Röding, 
1798, for two reasons. First, as Watson 
(1943) pointed out, the family Ellobiidae was, 
at the time of Gray's publication, divided into 
very few genera, and Carychium Müller, 
1774, Pythia Röding, 1798, and Auricula La- 
marck, 1799, all had been established many 
years earlier. Pythia had been introduced for 
Pythia helicina Röding [= Helix scarabeus 
Gmelin], a species which has a row of tuber- 
cles inside the outer lip. Group b of Gray's 
"Order 1 . Adelopneumona" included the am- 
phibious Auricula, Carychium and "Phytia." 
Gray's only example of "Phytia'' was Voluta 



denticulata Montagu, a form of Myosotella 
myosotis that also has two or more tubercles 
inside the outer lip. It can be assumed, there- 
fore, that Gray was including Voluta denticu- 
lata Montagu within the already known genus 
Pythia Röding on the basis of the dentition of 
the outer lip. Second, Gray's publication is 
notorious for the number of misspellings it 
contains. For example, in the first nine lines 
of page 231, on which "Phytia" appears in 
the fifth line, one can read: Clauselia [= Clau- 
silia], Ancillus [= Ancilus] and Phaneropneu- 
mana [= Phaneropneumona] and, near the 
bottom of the page, Neritino [= Neritina]. Fur- 
thermore, Gray (1847a) corrected "Phytia" to 
Pythia. In view of the above, "Phytia" of Gray 
must be treated as a misspelling of Pythia 
Röding, in accordance with Articles 19 and 
32 ii of the ICZN, and as such it lacks taxo- 
nomic standing. Gray's misspelling was later 
misspelled by Blainville (1824) and Deshayes 
(1832). 

Gray (1847a) also introduced Alexia for Vo- 
luta denticulata Montagu [= Auricula myoso- 
tis Draparnaud]. Stephens (1835) had used 
the same name for a genus of Coleóptera, 
however, rendering Gray's name preoccu- 
pied. This fact prompted Wenz (1920) to pro- 
pose Nealexia as a new name for /A/ex/a Gray, 
but Myosotella Monterosato, 1906, has pre- 
cedence over Wenz' name. 

In two more instances Gray made mistakes 
concerning Ovatella [= sensu Myosotella]. In 
1840 he used Ovatella Bivona as a subgenus 
of Conovulus Lamarck for Voluta denticulata 
Montagu; later (1847a) he included "Ovatella 
Gray non Bivona" in the synonymy of his Al- 
exia. Because Voluta denticulata was not in- 
cluded in Bivona's (1832) original species, 
"Ovatella 'Bivona' Gray" must be treated as 
a misuse of Ovatella Bivona. Gray (1847a) 
also included in the synonymy of his Alexia 
the name Jaminia Brown, 1827, but the latter 
name was preoccupied by Jaminia Risso 
(1826). 

Pallary (1900) proposed Kochia as a sub- 
genus o] Alexia Gray and he included, among 
other species. Alexia (K.) denticulata (Mon- 
tagu) and Alexia (K.) oranica Pallary [both 
junior synonyms of Myosotella myosotis 
(Draparnaud)]. The latter species was se- 
lected as type species by Monterosato 
(1906). Pallary (1921), unaware of Montero- 
sato's selection, proposed Alexia (K.) dentic- 
ulata as the type species of Kochia, noting at 
the same time that this name was preoccu- 
pied by Kochia Freeh (1891). 



194 



MARTINS 



Monterosato (1906) considered Montagu's 
Voluta denticulata and Draparnaud's Лил/си/а 
myosotis not only as being different species, 
but as belonging to different genera. Leaving 
the former within Gray's Alexia, he included 
the latter within his genus Myosotella, which 
he created for a group of species under 
Pfeiffer's Alexia #2 (1856a: 147); he desig- 
nated Myosotella payraudeaui ("Shuttle- 
worth" Pfeiffer, 1 856) as the type species. On 
the basis of Pfeiffer's description, I consider 
Myosotella payraudeaui conspecific with My- 
osotella myosotis (Draparnaud). Monterosa- 
to's name, then, is the earliest available name 
for the subgenus that includes Myosotella 
myosotis (Draparnaud). 

Habitat: Myosotella lives mainly above the 
high-tide mark, sometimes even away from 
the influence of spring tides (Morton, 1955b). 

Range: Although it has a worldwide distribu- 
tion Myosotella is generally absent from the 
tropics. 

Myosotella myosotis (Draparnaud, 1801) 
Figs. 41-84 

Auricula myosotis Draparnaud, 1801: 53 
[Mediterranean coast; type probably in 
Vienna (Locard, 1895)]; Draparnaud, 
1805: 56, pi. 3, figs. 16, 17; Férussac, 
1821: 103; Lamarck, 1822, 6: 140; Blain- 
ville, 1824: 246; Blainville, 1825: 453, pi. 
37 bis, fig. 6; Gould, 1833: 67; Griffith & 
Pidgeon, 1834: 36; Küster, 1844: 19, pi. 
1, figs. 15-17; Moquin-Tandon, 1851: 
348-351 [anatomy]. 

Voluta denticulata Montagu, 1803: 234, pi. 
20, fig. 5 [Devon, England; lectotype 
herein selected RAMM 4100 (Fig. 41); 
paralectotypes RAMM 4100]; Dillwyn, 
1817: 506; Wood, 1825: 90, pi. 19, fig. 
18. 

Voluta ringens Turton, 1819: 250 [England; 
lectotype herein selected USNM 85901 1 
(Fig. 42); paralectotype USNM 55351]. 

Voluta reflexa Turton, 1819: 251 [Exmouth, 
England; holotype USNM 55370 (Fig. 
44)]. 

Phytia denticulata (Montagu). Gray, 1821: 
132; Gardiner, 1923: 64; Germain, 1931: 
561, text fig. 597. 

Auricula véneta Von Martens, 1824: 433 
[Venice: location of type unknown (fide 
Cesari, 1976)]. 

Jaminia denticulata (Montagu). Brown, 1827, 
pi. 51, fig. 6. 



Jaminia quinquedens Brown 1827, pi. 51, fig. 
1 1 [Prestonpans, England; type probably 
at Manchester (Sherborn, 1940)]. 

Acteon denticulatus (Montagu). Fleming, 
1828: 337. 

Auricula tenella Menke, 1828: 36 [Type local- 
ity herein designated to be Norderney Is- 
land; location of type unknown]; Menke, 
1830: 131; Küster, 1844: 57. 

Carychium personatum Michaud, 1831: 73, 
pi. 15, figs. 42, 43 [Bretagne, France; 
lectotype herein selected MNHNP (Fig. 
45)]. 

Melampus borealis Conrad, 1832: 345 [New- 
port, Rhode Island; type material pre- 
sumed lost (Baker, 1964)]; Jay, 1839: 59; 
H. & A. Adams, 1854: 10. 

Melampus gracilis Lowe, 1832: 288 [Madeira; 
location of type unknown]. 

Auricula myosotis Lamarck. Orbigny, 1835: 
23. 

Pythia denticulata (Montagu) Gray. Beck, 
1837: 103. 

Pythia myosotis (Draparnaud). Beck, 1837: 
104. 

Auricula reflexilabris Orbigny, 1837: 326, pi. 
42, figs. 1-3 [Lima, Peru; lectotype 
herein selected BMNH 1854.12.4.242 
(Fig. 46)]. 

Auricula (Auricula) myosotis (Draparnaud). 
Anton, 1839: 48. 

Auricula denticulata (Montagu). Gould, 1841: 
199, fig. 129; De Kay, 1843: 58, pi. 5, fig. 
93; Küster, 1844: 54, pi. 8, figs. 1-5; 
Reeve, 1877, pi. 7, fig. 61. 

Auricula mysotis Draparnaud. Sowerby, 
1842: 99 [misspelling oi myosotis]. 

Auricula denticulata var. borealis (Conrad). 
De Kay, 1843: 58, pi. 5. fig. 91. 

1 Auricula sayi Küster, 1844: 42, pi. 6, figs. 14, 
15 [United States of America; location of 
type unknown {nomen dubium)]. 

Auricula microstoma Küster, 1844: 52, pi. 1, 
figs. 18, 19 [Budua, Dalmatia; location of 
type unknown]. 

Auricula kutschigiana Küster, 1844: 54, pi. 8, 
figs. 11-14 [Servóla near Trieste; Lissa 
Island; location of type unknown]. 

Auricula biasolettiana Küster, 1844: 56, pi. 8, 
figs. 18-20 [Niza; Trieste; coast of Dal- 
matia; location of type unknown]. 

Auricula myosotis var. elongata Küster, 1 844: 
69, pi. 8, figs. 21, 22 [Zara; location of 
type unknown]. 

Auricula myosotis var. adriatica Küster, 1 844: 
69, pi. 8, figs. 23, 24 [Trieste; Istria; Dal- 
matia; Zara; location of type unknown]. 



WESTERN ATLANTIC ELLOBIIDAE 



195 



Aurícula ciliata Morelet, 1845: 77, pi. 7, fig. 4 
[Alcacer do Sal, Alentejo, Portugal; lec- 
totype herein selected BMNH 
1893.2.4.831 (Fig. 47)]. 

Aurícula botteríana Philippi, 1846: 97 [Lésina 
Island, Dalmatia; location of type un- 
known]. 

Melampus denticulatus auct. Stimpson, 
1851: 52. 

Alexia denticulata (Montagu). Leach, 1852: 
97; Locard, 1882: 182; Adam, 1947: 39; 
Sevo, 1974: 5, fig. 5. 

Alexia obsoleta Pfeiffer, 1854a: 1 1 1 [Tergesti, 
Adriatic Sea; location of type unknown]; 
Kobelt, 1898: 131, pi. 19, figs. 5, 6. 

Alexia myosotis (Draparnaud). Pfeiffer 
1854b: 151; Pfeiffer, 1856a: 148; Binney 
1859: 172, pi. 75, fig. 33, pi. 79, fig. 16 
Binney, 1860: 4; Binney, 1865: 4, figs 
2-4; Tryon, 1866: 6, pi. 18, figs. 1, 2 
Pfeiffer, 1876: 365; Nevill, 1879: 227 
Verrill, 1880: 250; Locard, 1882: 183 
Apgar, 1891: 130; Schneider, 1892: 116 
Whiteaves, 1901: 208; C.W. Johnson 
1915:1 78; Morse, 1 921 : 21 , pi. 7, fig. 44: 
Nobre, 1930: 165, pi. 7, fig. 70; Nobre 
1940: 36; Adann, 1947; 38; La Rocque 
1953: 262; Porter, 1974: 300; Sevo 
1974: 6, fig. 6. 

Conovulus denticulatus (Montagu). Clark, 
1855: 297. 

Alexia bermudensis H. & A. Adams, 1855a: 
33 [Bermuda; lectotype herein selected 
BMNH 1969105 (Fig. 48)]: H. & A. Ad- 
ams, 1855b: 241; Pfeiffer, 1856a: 152; 
Pfeiffer, 1876: 367; Kobelt, 1901: 282, pi. 
33, fig. 3; Fénaux, 1939: 43, pi. 1, fig. 6. 

Conovulus (Alexia) denticulata (Montagu). 
Woodward, 1856: 174. 

Alexia payraudeaui "Shuttleworth" Pfeiffer, 
1856a: 147 [Corsica; Nizza; Tergesti; lo- 
cation of type unkown]; Pfeiffer, 1876: 
365; Kobelt, 1898; 130, pi. 17, figs. 21, 
22. 

Melampus tumtus (Say MS) Binney, 1859: 
174 [Rhode Island; type presumably de- 
posited at ANSP, probably lost]. 

Aurícula bicolor Morelet, 1860: 206, pi. 5, fig. 
7 [Pico, Azores; lectotype herein se- 
lected BMNH 1893.2.4.822 (Fig. 49)]. 

Aurícula vespertina Morelet, 1860: 210, pi. 5, 
fig. 9 [Pico, Azores; lectotype herein se- 
lected BMNH 1893.2.4.825 (Fig. 50)]. 

Alexia micheli Bourguignat, 1864: 140, pi. 8, 
figs. 34-36 [La Calle and Cherchell, Al- 
geria; lectotype herein selected MHNG 
(Fig. 51)]. Non Mittré, 1841. 



Alexia micheli var. tnplicata Bourguignat, 
1864; 141, pi. 8, figs. 37, 38 [La Calle, 
Algeria; lectotype herein selected MHNG 
(Fig. 52)]. 

Alexia algeríca Bourguignat, 1864: 141, pi. 8, 
figs. 23-26 [Algeria; lectotype herein se- 
lected MHNG (Fig. 53)]; Kobelt, 1898: 
128, pi. 17, figs. 18, 19. 

Alexia algeríca var. quadríplicata Bourguig- 
nat, 1864: 142, pi. 8, figs. 27-30 [Algeria; 
lectotype herein selected MHNG (Fig. 
54)]. 

Alexia loweana Pfeiffer, 1866: 145 [Madeira 
Island; location of type unknown]. 

Melampus myosotis (Draparnaud). Jeffreys, 
1869: 106, pi. 4, fig. 2 [Voluta ríngens 
Turton illustrated (Fig. 43), probably type 
material]. 

Alexia setifer Cooper, 1872: 153, pi. 3, figs. 
AI -A3, A5-A6 [San Francisco Bay, 
California; holotype ANSP 22513a (Fig. 
55)]. 

Alexia setifer var. tenuis Cooper, 1872: 154, 
pi. 3, fig. A4 [San Francisco Bay, Califor- 
nia; holotype ANSP 22513b (Fig. 56)]. 

Alexia (Aurícula) myosotis var. hiriarti Follin & 
Béhllon, 1874; 88 [Biarritz lighthouse; 
lectotype herein selected MNHNP (Fig. 
57)]. 

Alexia setigera Cooper. Pfeiffer, 1876: 368; 
Fénaux, 1939: 43 [error for setifer]. 

Aurícula (Alexia) meridionalis Brazier, 1877: 
26 [Port Adelaide, South Australia; holo- 
type ANSP 22506a (Fig. 58)]. 

Auricula watsoni Wollaston, 1878: 269 [Ma- 
deira; lectotype herein selected BMNH 
1895.2.2.411 (Fig. 59)]. 

Aurícula watsoni scrobiculata Wollaston, 
1878: 269 [Salvages Islands (Madeira); 
lectotype herein selected BMNH 1895. 
2.2.417 (Fig. 60)]. 

Aurícula bicolor var. subarmata Wollaston, 
1878: 466 [Lanzarote (Canary Islands); 
location of type unknown]. 

Aurícula (Alexia) denticulata (Montagu). Fisch- 
er, 1878: 309-312. 

Alexia setífera Cooper. Nevill, 1879: 226 [un- 
justified emendation of setifer]. 

Alexia borealis Say Cooper. Nevill, 1879: 227. 

Alexia tiiriarti Follin & Bérillon. Locard, 1882: 
183. 

Alexia biasoletina (Küster). Locard, 1882: 183 
[misspelling of biasolettiana]. 

Alexia ciliata (Morelet). Locard, 1882: 184; 
Kobelt, 1898: 129, pi. 17, fig. 20. 

Tralla (Alexia) myosotis (Draparnaud). Dall, 
1885: 277; Dall, 1889: 92, pi. 52, fig. 9. 



196 



MARTINS 



Tralia (Alexia) myosotis var. ringens (Turton). 
Dali, 1885: 278. 

Tralia (Alexia) myosotis forma junior Dali, 
1885: 278 [new name for Auricula ciliata 
Morelet and Alexia setifer Cooper]. 

Alexia cossoni Letour neux & Bourguignat, 
1887: 130 [Gabès and Cheiba, Cape 
Bon, Tunisia; lectotype herein selected 
MHNG (Fig. 61)]. 

Alexia terrestris Letourneux & Bourguignat, 
1887: 130 [El-Hamma, S of Gabès, Tu- 
nisia; holotype MHNG (Fig. 62)]. 

Alexia globulus Bourguignat, in Letourneux & 
Bourguignat, 1887: 131 [Gabès, Tunisia; 
holotype MHNG (Fig. 63); on museum la- 
bel as Alexia ovum Bourguignat]. 

Alexia letourneuxi Bourguignat, in Letourneux 
& Bourguignat, 1887: 131 [Mandara, 
near Alexandria, Egypt, and Djerba Is- 
land, Tunisia; lectotype herein selected 
MHNG (Fig. 64)]. 

Alexia pechaudi Bourguignat, in Letourneux 
& Bourguignat, 1887: 132 [Macta near 
Gran and Mdjerda, Tunisia; holotype 
MHNG (Fig. 65)]. 

Alexia acuminata Morelet, 1889: 15, pi. 1, fig. 
11 [Port Elizabeth, Cape Colony, South 
Africa; specimen marked "type" broken, 
lectotype herein selected BMNH 
1893.2.4.838 (Fig. 66)]. 

Alexia pulchella Morelet, 1889: 15, pi. 1, fig. 
10 [Port Elizabeth, Cape Colony, South 
Africa; lectotype herein selected BMNH 
1911.8.8.39 (Fig. 67)]. 

Alexia armoricana Locard, 1891: 132 [west 
coast of France; lectotype herein se- 
lected MNHNP (Fig. 68)]. 

Alexia exilis Locard, 1893: 62 [Le Croisic, 
Loire-Inférieure; Porquerolles (France); 
herein restricted to Porquerolles; lecto- 
type herein selected MNHNP (Fig. 69)]. 

Alexia parva Locard, 1893: 62 [Le Croisic, 
Loire-lnfèheure (France); lectotype here- 
in selected MNHNP (Fig. 70)]. 

Alexia ringicula Locard, 1893: 62 [Arrdudon, 
Morbihan (France); lectotype herein se- 
lected MNHNP (Fig. 71)]. 

Auricula (Alexia) myosotis Draparnaud. 
Pelseneer, 1894a: 73, figs. 195-208 
[anatomy]. 

Alexia Ь/со/ол (Morelet). Kobelt, 1898: 134, pi. 
24, fig. 3. 

Alexia vespertina (Morelet). Kobelt, 1898: 
135, pi. 24, fig. 4. 

Alexia (Kochia) oranica Pallary, 1900: 240, pi. 
6, figs, 2, 2a [Gran, Tunisia; lectotype 
herein selected MNHNP (Fig. 72)]. 



Alexia myosotis marylandica Pilsbry, 1900a: 
40 [Mouth of St. Leonards Creek, Patux- 
ent River, Maryland; lectotype by Baker 
(1964) ANSP 22483a (Fig. 73)]; C.W. 
Johnson, 1934: 159. 

Alexia myosotis bermudensis Pfeiffer. Pilsbry, 
1900b: 504. 

Alexia oranica Pallary. Kobelt, 1901: 280, pi. 
31, figs. 8, 9. 

Alexia bidentata Montagu forma americana 
Kobelt, 1901: 312, pi. 33, figs. 1,2 [Ber- 
muda; type Senckenberg Museum, 
Frankfurt-am-Main (not seen)]. 

Myosotella myosotis (Draparnaud). Montero- 
sato, 1906: 126. 

Phytia myosotis var. bermudensis (H. & A. 
Adams). Peile, 1926: 88. 

Phytia myosotis (Draparnaud). Ellis, 1926: 96, 
pi. 2, fig. 3, pi. 5, fig. 49; Germain, 1931: 
560, text figs. 295, 296, pi. 18, figs. 535, 
536; McMillan, 1947: 264; McMillan, 
1 949: 67; M. Smith, 1 951 : 1 45, pi. 55, fig. 
3, pi. 71, fig. 9; McMillan, 1968: 165; 
Climo, 1982: 43-48, fig. 1, A-L 

Alexia (Myosotella) myosotis (Draparnaud). 
Thiele, 1931: 466. 

Phytia myosotis myosotis (Draparnaud). 
Winckworth, 1932: 238. 

Phytia myosotis denticulata (Montagu). 
Winckworth, 1932: 238. 

Alexia myosotis myosotis (Draparnaud). C.W. 
Johnson, 1934: 159. 

Alexia myosotis var. varicosa Pénaux, 1939: 
44, pi. 1, fig. 3 [Provence, France; type 
probably in Fènaux's collection, École 
des Mines, Paris]. 

Alexia subflava Pénaux, 1939: 45, pi. 1, fig. 9 
[Bermuda; type in Fènaux's collection, 
École des Mines, Paris (not seen)]. 

Phytia bermudensis (H. & A. Adams). Morri- 
son, 1951b: 10. 

Phytia myosotis marylandica (Pilsbry). Morri- 
son, 1951b: 10; Burch, 1960a: 182 
[chromosomes]. 

Phytia myosotis borealis (Conrad). Morrison, 
1951b: 10. 

Ovatella myosotis (Draparnaud). Meyer, 
1955: 1-43, pis. 1, 2 [anatomy, taxon- 
omy, life history]; Morton, 1955b: 119- 
131, figs, [anatomy, life history]; Morton, 
1955c: 127-168 [anatomy, taxonomy, 
evolutionary relationships]; Bousfield, 
1960: 14, pi. 1, fig. 10; Coomans, 1962: 
90; Kensler, 1967: 391-406 [ecology]; 
Jacobson & Emerson, 1 971 : 65, text fig.; 
Baranowski, 1971: 143; Abbott, 1974: 
334, fig. 4103; Emerson & Jacobson, 



WESTERN ATLANTIC ELLOBIIDAE 



197 



1976: 192, pi. 26, fig. 28; Hubendick, 
1978: 1-45 [taxonomic relationships]; 
Morrell, 1980: 208-209; Rehder, 1981: 
650, fig. 232; Jensen & Clark, 1986: 458, 
figured. 

Ovatella (Myosotella) myosotis (Draparnaud). 
Ziich, 1959: 73, fig. 236; Cesari, 1973: 
181-210 [taxonomy, distribution, ecol- 
ogy]; Giusti, 1973: 124, figs. 4 A-N, pi. 2, 
figs. 1-4, pi. 3, figs. 1-3; Giusti, 1976; 
Cesari, 1976: 3-19, 5 pis. [taxonomy, 
anatomy, polymorphism]; Martins, 1978: 
24, pi. 3, figs. 4, 4a, 4b, pi. 4, figs. 4, 4a, 
4b, pi. 5, figs. 5, 6, D; Martins, 1980: 
1-24, pi. 2, figs, f-o [habitat]. 

Ovatella (Alexia) myosotis (Draparnaud). Rus- 
sell-Hunter & Brown, 1964: 134. 

Ovatella myosotis bermudensis (H. & A. Ad- 
ams). Abbott, 1974: 334 [fig. 4105, erro- 
neously stated to be Microtralia occiden- 
talis, appears to be Myosotella myosotis 
from Bermuda]. 

Description: Shell (Figs. 41-77) to 12 mm 
long, oval-elongate, fragile to somewhat 
solid, commonly pale yellow to purplish red, 
rarely whitish. Spire high, with as many as 
eight somewhat convex whorls; first three 
whorls of teleoconch with spiral rows of pits, 
becoming fewer as spire progresses (Figs. 
76, 77); row of hairs, in juveniles, anterior to 
spiral rows of pits (Fig. 77). Body whorl about 
70% of shell length, smooth except for faint, 
irregularly spaced growth lines. Aperture 
about 80% body whorl length, oval-elongate, 
anteriorly rounded; inner lip with small, very 
oblique and somewhat twisted, white col- 



umellar tooth; anterior parietal tooth stron- 
gest, white, of variable thickness and perpen- 
dicular to columellar axis; usually one, rarely 
none, sometimes as many as four posterior 
parietal teeth that gradually become smaller 
posteriorly; outer lip sharp, often weakly re- 
flected in gerontic specimens, commonly 
with one, sometimes with as many as six 
whitish tubercles. Partition of inner whorls 
only in body whorl (Fig. 75). Protoconch as in 
genus. 

Animal grayish white to yellowish brown; 
neck usually darkly pigmented; tentacles 
subcylindhc, darker than neck; rudimentary 
anterior tentacles present; foot not trans- 
versely divided, yellowish; mantle skirt gray- 
ish with dark spots. 

Radula (Figs. 78-80) having formula (20 + 
11 +1 +11 + 20) X 80. Width of central tooth 
base twice that of lateral teeth, with central 
emargination, anterior portion of arms some- 
what sinuous; crown small, posteriorly de- 
pressed, unicuspid; mesocone triangular, 
somewhat rounded. Lateral teeth eight to 13; 
base quadrangular, elongate, oblique, with 
rounded lateral prominence over anterior 
third; crown cuneiform, about half length of 
base, posteriorly rounded. Marginal teeth 17 
to 25; base becoming reduced anteriorly, 
projecting and square posteriorly; crown 
pointing medially, bicuspid; endocone some- 
what smaller than mesocone. 

Stomach with anterior membranous cham- 
ber, median muscular gizzard and posterior 
membranous gastric caecum (Fig. 81). 

Reproductive system (Fig. 82) with ovotes- 



FIGS. 41-60. Myosotella myosotis (Draparnaud). (41) Voluta denticulata Montagu, lectotype (RAMM 4100), 
Devon, England, si 8.5 mm. (42) Voluta ringens Turton, lectotype (USNM 859011), British Isles, si 8.4 mm. 

(43) Voluta ringens Turton, figured in Jeffreys' British Conchology, pi. 98, fig. 29 (USNM 67947), si 8.5 mm. 

(44) Voluta reflexa Turton, hoiotype (USNM 55370), British Isles, si 9.2 mm. (45) Carychium personatum 
Mictnaud, lectotype (MNHNP), Boulogne, France, si 6.5 mm. (46) Auricula reflexilabris Orbigny, lectotype 
(BMNH 1854.12,4.242), Lima, Peru, si 9.0 mm. (47) Auricula ciliata Morelet, lectotype (BMNH 1893.2.4.831), 
Portugal, si 7.8 mm. (48) Alexia bernnudensis H. & A. Adams, lectotype (BMNH 1969105), locality not given 
[Bermuda], si 7.6 mm. (49) Auricula bicolor Morelet, lectotype (BMNH 1893.2.4.822), Pico, Azores, si 9.7 
mm. (50) Auricula vespertina Morelet, lectotype (BMNH 1893.2.4.825), Area [Areia] Larga, Pico, Azores, si 
7.8 mm. {5^) Alexia mictieii Bourguignat, lectotype (MHNG), La Calle, Algeria, si 9.2 mm. (52) Alexia nnichieli 
var. triplicata Bourguignat, lectotype (MHNG), La Calle, Algeria, si 8.0 mm. (53) Alexia algerica Bourguignat, 
lectotype (MNHG), Mostaghanem, Algeria, si 9.4 mm. (54) Alexia algerica var. quadriplicata Bourguignat, 
lectotype (MHNG), Cape Caxine near Alger, Algeria, si 6.8 mm. (55) Alexia setifer Cooper, hoiotype (ANSP 
22513a), San Francisco, California, si 7.1 mm. (56) Alexia setifer var. tenuis Cooper, hoiotype (ANSP 
22513b), San Francisco, California, si 6.4 mm; Baker (1964) gave the length as 7.7 mm, which does not 
match the length of the shell marked as type. (57) Alexia (Auricula) myosotis var. hiriarti Foiiin & Bériilon, 
lectotype (MNHNP), Biarhtz lighthouse, France, si 10.1 mm. (58) Auricula (Alexia) meridionalis Brazier, 
hoiotype (ANSP 22506a), Port Adelaide, South Australia, si 8.3 mm. (59) Auricula watsoni Wollaston, 
lectotype (BMNH 1895.2.2.411), Madeira, si 8.1 mm. (60) Auricula vt/atsoni scrobiculata Wollaston, lecto- 
type (BMNH 1895.2.2.417), Salvages Islands [Madeira], si 7.5 mm. 



198 



MARTINS 




FIGS. 41-60. 



WESTERN ATLANTIC ELLOBIIDAE 



199 




FIGS. 61-77. 



200 



MARTINS 




FIGS. 78, 79. Myosotella myosotis, radular teeth, Newport River, North Carolina, si 5.1 mm. Scale 100 цт. 



tis light colored, between lobes of digestive 
gland; hermaphroditic duct long, dilated, 
convoluted; palliai gonoduct hermaphroditic 
along its entire length; anterior mucous gland 
and prostate gland cover entire length of 
spermoviduct; bursa duct as long as sper- 
moviduct, emptying near vaginal opening; 
spermatheca spherical. Penis short, thick; 
associated vas deferens adhering to penis. 

Nervous system (Fig. 83) with cerebral 
commissure one and one-half times width of 
cerebral ganglion; left and right cerebropleu- 
ral and cerebropedal connectives of same 



length; connectives of visceral nerve ring 
long; right pleuroparietal connective twice as 
long as left one; left parietovisceral connec- 
tive longer than right one, sometimes with 
ganglionic swelling on anterior third, from 
which internal palliai nerve originates; rudi- 
mentary osphradial ganglion arising from 
pneumostomal nerve. 

Remarks: Myosotella myosotis is an ex- 
tremely variable species especially known 
from European coasts. Within one population 
the shape of the shell can vary from slim and 



FIGS. 61-77. Myosotella myosotis (Draparnaud). (61) Alexia cossoni Letourneux & Bourguignat, lectotype 
(MHNG), Lagune de l'oued Cheiba, (Cap Bon), Tunisia, si 7.3 mm. (62) Alexia terrestris Letourneux & 
Bourguignat, holotype (MHNG), El Hamma, S of Gabès, Tunisia, si 5.4 mm. (63) Alexia globulus Bourguig- 
nat, holotype (MHNG), Gabès, Tunisia, si 5.7 mm. (64) Alexia letoumeuxi Bourguignat, lectotype (MHNG), 
Mandara, near Alexandria, Egypt, si 5.7 mm. (65) Alexia pechaudi Bourguignat, holotype (MHNG), La 
Mactra, near Gran, Tunisia, si 5.2 mm. (66) Alexia acuminata Morelet, lectotype (BMNH 1893.2.4.838), 
Natal, si 5.0 mm. (67) Alexia pulchella Morelet, lectotype (BMNH 191 1 .8.8.39), Port Elizabeth, South Africa, 
si 5.0 mm. (68) Alexia armoricana Locard, lectotype (MNHNP) Brest, Finisterre, France, si 5.1 mm. (69) 
Alexia exilis Locard, lectotype (MNHNP), Porquerolles, France, si 6.1 mm. (70) Alexia parva Locard, lecto- 
type (MNHNP), Le Croisic, Loire-Inférieure, France, si 5.0 mm. (71) Alexia ringicula Locard, lectotype 
(MNHNP), Arrdudon, Morbihan, France, si 5.0 mm. (72) Alexia (Kochia) oranica Pallary, lectotype (MNHNP), 
Oran, Tunisia, si 6.0 mm. (73) Alexia myosotis marylandica Pilsbry, lectotype (ANSP 22483a) Patuxent River, 
Maryland, si 8.0 mm. (74) Jamestown, Rhode Island, si 6.7 mm. (75) Old Road, Shelly Bay, Bermuda, si 6.3 
mm. (76) Lateral view of spire and protoconch, Jamestown, Rhode Island. (77) Top view of spire and 
protoconch, Sao Miguel, Azores. Scale 1 mm. 



WESTERN ATLANTIC ELLOBIIDAE 



201 



с 1L 2L 10L 11L Ш 2M 3M 14M 15M 




FIG. 80. Myosotella myosotis, radula, Beaufort, 
North Carolina. Scale 10 ).im. 



....4/VV4Í er 




FIG. 81. Myosotella myosotis, stomach, Bermuda. 
Scale 1 mm. 



high spired to globose, and the color ranges 
from pale yellow to purplish red (Martins, per- 
sonal observations in Bermuda and Azores). 
Similar variability occurs in the apertural mor- 
phology, in which the number of parietal and 
outer lip teeth can vary considerably. It was 
the variability of these characters that evoked 
most of the many names given to this spe- 
cies. According to Locard (1895), Drapar- 
naud (1801) was aware of this variability 
when he described Auricula myosotis, be- 
cause the 113 syntypes included examples 
of the dentate form later described by Mon- 
tagu (1803) as Voluta denticulata. Michaud 
(1831), who completed Draparnaud's work, 
described Montagu's form as Carychium 
personatum (Fig. 45). 

Even quite recently the question of the con- 
specificity of the European forms included in 
the genus Myosotella has been extensively 




FIG. 82. Myosotella myosotis, reproductive sys- 
tem, Bermuda. A-C, transverse sections and their 
locations. Scale 1 mm. 



pfg2. prgl 




FIG. 83. Myosotella myosotis, central nervous sys- 
tem, Bermuda. Scale 1 mm. 



debated. Germain (1931) accepted two Eu- 
ropean species, Phytia myosotis (Drapar- 
naud), with only one posterior parietal tooth, 
and Phytia denticulata (Montagu), with a 
heavily dentate aperture. Winckworth (1932) 
treated both as subspecies of Phytia. Watson 
(1943) noted the differences between the two 
forms but added that there are intermediates. 
The slight differences he found in radular fea- 
tures could be explained by the different sizes 
of the specimens studied, and the differences 
in shell morphology could be attributed to the 



202 



MARTINS 



more saline habitat of Phytia denticulata. 
Pénaux (1939), after examining hundreds of 
specimens from a stretch of coast between 
Toulon and Agde, southern France, found al- 
most all the "species" described from Eu- 
rope. Cesari (1973) was inclined to treat Ova- 
tella denticulata as a synonym of Ovatella 
myosotis but later (1976), as did Watson 
(1943), he considered the case of Ovatella 
denticulata unclear pending a definite ana- 
tomical comparison. Considering the high de- 
gree of shell variability of Myosotella myosotis 
(sensu lato), a wide range of anatomical vari- 
ability is to be expected. The same condition 
is found in the Western Atlantic Melampus (M.) 
bidentatus, which exhibits high variability in 
shell morphology as well as in anatomical 
characters (see the remarks under that spe- 
cies). On the basis of the great range of vari- 
ability in shell morphology, I think it justifiable 
to consider Myosotella myosotis as the only 
species living in Europe and North Africa. The 
names Voluta ringens Turton, Voluta reflexa 
Turton, Auricula tenella Menke, Carychium 
personatum Michaud, Auricula botteriana 
Philippi, Alexia letourneuxi Bourguignat, Al- 
exia armoricana Locard, Alexia ringicula Lo- 
card and Alexia oranica Pallary all pertain to 
the dentate morph of Myosotella myosotis. 

I have concluded previously (Martins, 
1978, 1980) \ba\ Auricula vespertina Morelet 
and Auricula bicolor Morelet from the Azores 
are conspecific with Myosotella myosotis. 
Upon inspection of the type material of Wol- 
laston's Auricula watsoni and Auricula wat- 
soni scrobiculata from Madeira (Figs. 59, 60) 
I also include them in the synonymy of Myo- 
sotella myosotis. 

Shell morphology can be affected by envi- 
ronmental factors. The Bermudian speci- 
mens (Figs. 48, 75) are larger and thicker than 
the specimens from New England (Fig. 74), 
but similar to those I found in North Carolina 
[Alexia myosotis marylandica Pilsbry (Fig. 73)] 
and in the Azores. The thickening and en- 
hanced color of the shell seen nearer the 
warm regions is also observed in Melampus 
(M.) bidentatus (see the remarks under the 
species), and should be considered an envi- 
ronmentally determined character of little 
taxonomic value. The names Alexia myosotis 
marylandica Pilsbry and Alexia bermudensis 
H. & A. Adams, the latter considered a sub- 
species by Abbott (1974), are obviously only 
morphological variations of Myosotella myo- 
sotis. Alexia subflava Pénaux, also from Ber- 
muda, was based upon a form with unusual 



apertural features, but it is clearly within the 
range of variation of Myosotella myosotis, 
and it too must be considered synonymous. 

Myosotella myosotis (Draparnaud) and Au- 
riculinella (L.) bidentata (Montagu, 1801) are 
often confused. The latter was erroneously 
reported from America and Bermuda. Dall's 
(1885) statement that Melampus (Leuconia) 
bidentatus (Montagu) [= Auriculinella (Leuco- 
phytia) bidentata (Montagu)] lived in America 
was based on Binney's remarks about Myo- 
sotella myosotis. Binney (1 859: 1 74), after de- 
scribing the animal, noted that it differed from 
H. & A. Adams' illustration of the animal of 
Alexia denticulata (1855b: pi. 82, fig. 5). He 
mentioned that, "from the exterior of the an- 
imal there appears no difference between it 
and Melampus bidentatus." Apparently Dall 
(1885) wrongly concluded that the species in 
question should also have the foot trans- 
versely divided, a characteristic shared by 
Melampus (M.) bidentatus and Auriculinella 
(L.) bidentata, but not by Myosotella myoso- 
tis. From Dall's description of Melampus 
(Leuconia) bidentatus (Montagu) it is clear 
that he was confused about differences be- 
tween the shell of Myosotella myosotis and 
that of Auriculinella (L.) bidentata. 

Kobelt (1901: 283) briefly described a sup- 
posedly biplicate variation of Alexia bermu- 
densis H. & A. Adams, to which he later (p. 
312, caption of pi. 33, figs. 1, 2) gave the 
name Alexia bidentata Montagu forma amer- 
icana. The illustration hardly differs from that 
oí Alexia bermudensis (pi. 33, fig. 3), which H. 
& A. Adams (1855a: 33) described as having 
"columella biplicata" (Figs. 48, 75). As noted 
above, Myosotella myosotis varies greatly in 
apertural morphology, especially in the con- 
spicuousness of the posterior parietal teeth. 
Alexia bidentata Montagu forma americana 
Kobelt is just a phenotypic variant of Myoso- 
tella myosotis. 

Three other names were applied to North 
American specimens. Küster (1844) de- 
scribed and figured an Auricula sayi. In the 
words of Binney (1 859: 1 78), "Küster's figure 
represents no known American shell. There 
exists, however, a strong resemblance be- 
tween it and his figure of Alexia myosotis." 
Pfeiffer (1856a) tentatively assigned Küster's 
name to Marinula, and compared it with Au- 
ricula infrequens С В. Adams, 1852, from 
Panama. After examining С В. Adam's type 
material I disagree with Pfeiffer's compari- 
son. The dentition shown in Küster's illustra- 
tion resembles that of Creedonia succinea, 



WESTERN ATLANTIC ELLOBIIDAE 



203 



although the shell is too globose and acumi- 
nate to be referred with certainty to that spe- 
cies. In view of the conflicting diagnostic 
characters derived from the illustration and 
from the description given by Küster, I con- 
sider Auricula sayi Küster a normen dubium. 

The other two problematic names are 
Melampus borealis Conrad and Melampus 
turritus (Say MS) Binney, both from Rhode 
Island, and both undoubtedly conspecific 
with Myosotella myosotis. The former was 
misidentified by Pfeiffer (1856a) who, based 
upon misidentified specimens from Georgia 
in the Cuming collection, wrongly assigned 
them to Melampus bidentatus Say, var. y bo- 
realis Conrad. Pfeiffer's description of this 
variety (1856a: 46) mentioned an "outer lip 
with a white callus, regularly with 6-10 pli- 
cae." Melampus (D.) floridanus, another 
Georgian species, has as many as ten riblets 
inside the outer lip, but it is doubtful that 
Pfeiffer, who had introduced the latter spe- 
cies 1 1 pages before, would have confused it 
with Myosotella myosotis. Melampus (M.) bi- 
dentatus normally exhibits the sort of dentic- 
ulation on the outer lip mentioned by Pfeiffer, 
but this feature never has been found in My- 
osotella myosotis. One must conclude that 
Pfeiffer relied on misidentified specimens 
when he identified his variety with Melampus 
borealis Conrad. The description of Melam- 
pus turritus, found by Binney (1859) among 
Say's unpublished manuscripts, was pub- 
lished by that author only to provide addi- 
tional information about Myosotella myosotis. 

Myosotella myosotis can be differentiated 
conchologically from Melampus (M.) bidenta- 
tus and Melampus (D.) floridanus, with which 
it associates, by its less globose shape, by its 
shorter, anteriorly rounded and wider aper- 
ture, and by its lack of riblets within the outer 
lip. It differs from Creedonia succinea by its 
pointed spire and by the dentition of its inner 
lip, which in Creedonia has a very strong, 
posteriorly located parietal tooth. Some 
dwarf, thin-shelled forms of Tralla (T.) ovula 
can be confused with the solid, deeply col- 
ored forms of Myosotella myosotis. This fact 
probably accounts for Dall's (1885) report of 
the latter species from Jamaica. The nonmu- 
cronate apex, the sinuous outer lip and the 
white, equidistant teeth of the inner lip of Tra- 
lla constitute sufficient diagnostic characters, 
however. Gerontic individuals of Myosotella 
myosotis have a weakly reflected outer lip, a 
feature that led early authors to insist on in- 
cluding this species in the genus Auricula. 



Detailed studies of life history and anatomy 
were published simultaneously by Morton 
(1955b) and Meyer (1955). 

Habitat: Myosotella myosotis lives in salt 
marshes and adjacent areas, preferring piles 
of rocks and detritus above the high-tide 
mark. In Bermuda this species commonly 
lives under piles of rocks, farther onto land 
than any other halophilic ellobiid, a situation 
also observed in the Azores (Marlins, 1980). 

Range: Myosotella myosotis is well known as 
a Mediterranean and Eastern Atlantic spe- 
cies. "Species" very similar to Myosotella 
myosotis have been described from extra- 
European shores, such as Orbigny's (1837) 
Auricula reflexilabris (Fig. 46) from the Pacific 
coast of South America, Cooper's (1872) Al- 
exia setifer (Figs. 55, 56) from California, Bra- 
zier's (1877) Auricula (Alexia) meridionalis 
(Fig. 58) from southern Australia and More- 
let's (1889) Alexia acuminata (Fig. 66) and Al- 
exia pulchella (Fig. 67) from South Africa. 
Hanna (1939) included Cooper's species 
among the "Exotic Mollusca in California" 
and I concur with Paulson (1957) in conclud- 
ing that the Californian Alexia setifer Cooper 
does not differ from eastern American or Eu- 
ropean specimens. Alexia setifer Cooper, as 
well as Auricula ciliata Morelet, were named 
on the basis of the presence of hairs on the 
spire of juveniles. Clark (1855) first noted that 
this condition occurs in Myosotella myosotis. 
Taking into consideration the well-docu- 
mented morphological plasticity shown by 
Myosotella myosotis, I concur with Climo 
(1982) in synonymizing Brazier's species, as 
well as the others just mentioned. 

The wide range of Myosotella myosotis is 
attributed to its estuahne and supralittoral 
habits; most probably the animals were car- 
ried about in ballast or as egg masses laid on 
deck equipment and cargo that came in di- 
rect contact with marsh communities (Climo, 
1982). 

In the Western Atlantic this species occurs 
from Halifax, Nova Scotia (Bousfield, 1960), 
to Georgia, Bermuda and Cuba (Fig. 84). The 
Cuban specimen at the USNM (383711) 
should be classed as a spurious report until 
further confirmation because it is far from the 
range of the species in the Western Atlantic. 
Dall's report of this species from Jamaica is 
doubtful and it has not been confirmed by 
recent collections. Stimpson (1851), followed 
by Binney (1859, 1865), Verrill (1880) and Dall 
(1885), remarked that this species probably 



204 



MARTINS 




FIG. 84. Myosotella myosotis, geographic distribu- 
tion, Western Atlantic. Open circle, locality from 
literature. 



was introduced to the eastern coast of North 
America. 

Specimens Examined: MAINE: Castine 
(MCZ 4180; USNM 492501); Portland (MCZ 
uncatalogued; USNM 24865, 73394); New- 
castle (MCZ 34005). NEW HAMPSHIRE: 
Fabian Point, Great Bay, Newington (R.B.). 
MASSACHUSETTS (ANSP 22508; USNM 
27740, 27913): Manchester (USNM 39800) 
Marblehead (MCZ 199478; USNM 492503) 
Boston (MCZ uncatalogued; USNM 41240) 
Woods Hole (ANSP 357609; MCZ 34004 
USNM 158953, 525155); New Bedford 
(ANSP 22494; MCZ uncatalogued; USNM 
139801). RHODE ISLAND (MCZ 34003; 
USNM 539238): Newport (MCZ 68946, 
163167; USNM 39799, 67730); Warren 
(ANSP 60355); Maple Creek, Jannestown 
(A.M.); Wickford (MCZ 294645). CONNECTI- 
CUT: Branford (MCZ 34847; USNM 492502); 
New Haven (USNM 83471). NEW YORK: 
New York Harbor (USNM 492485); Cold 
Spring Harbor (MCZ 294167); Staten Island 
(MCZ 56738, 61847, 119477; USNM 59729, 
407787, 492500). NEW JERSEY: Cape May 
(MCZ uncatalogued). MARYLAND: Patuxent 
River (ANSP 22483. 3591 54; USNM 492486); 



St. Leonards Creek, Patuxent River (ANSP 
60971; USNM 465806); Chsfield (USNM 
618924). VIRGINIA: Mollusk (USNM 791448); 
Watts Bay (USNM 701628); Chincoteague Is- 
land (MCZ uncatalogued); Fisherman's Island 
(USNM 422292); Norfolk (USNM 637142). 
NORTH CAROLINA: mouth of Newport River, 
S of Beaufort (A.M.). SOUTH CAROLINA: 
Charleston (MCZ uncatalogued); McClellan- 
ville (USNM 663059). GEORGIA: Isle of Hope 
(USNM 663053); Thunderbolt (USNM 
663055). BERMUDA (ANSP 48594, 48595, 
48596, 62743, 78217, 79937, 85588; MCZ 
8972, 9971, 24407, 24408, 24409, 294163, 
294166; USNM 6529a, 6537, 94436, 94437, 
101401, 151271, 250298a, 492487, 492488, 
482490): Hamilton (USNM 152134, 171941); 
Hamilton Beach (MCZ uncatalogued); Fairy- 
land (ANSP 99074; USNM 208070); Gibbet 
Island (MCZ 294162); Flatts (ANSP 88572; 
MCZ 294164; USNM 1719340); Shelly Bay 
(MCZ 294165; USNM 492489); Old Road, 
Shelly Bay (A.M.); N of Shelly Bay Beach 
(A.M.); S of Coney Island (R.B.); Ferry Reach 
Park (R.B.); N of Long Bird Bridge (A.M.); 
Castle Harbour (ANSP 143320); Cooper's Is- 
land (ANSP 131644); Spitall Pond (A.M.); 
Hungry Bay (ANSP 88580; USNM 171947; 
A.M.); Paget (USNM 71 4209); W of Somerset 
Bridge (A.M.); S of Ely's Harbour (A.M.); Man- 
grove Bay (A.M.). CUBA: Los Canos, Guan- 
tánamo (USNM 383711). 

Genus Laemodonta Philippi, 1846 

Laemodonta Philippi, 1846: 98. Type species 
by monotypy: Laemodonta [Auricula] 
striata (Philippi, 1846) [= Pedipes octan- 
fracta Jonas, 1845]. Non Martens, 1824, 
nee Anton, 1839. 

Laimodonta Bronn, 1847: 4 [nomen nudum, 
fide Herrmannsen, 1852]. Non "Nuttall" 
H. & A. Adams, 1855a. 

Plecotrema H. & A. Adams, 1853: 120. Type 
species by original designation: Ple- 
cotrema typica H. & A. Adams, 1853. 

Bullapex Haas, 1950: 199. Type species 
by monotypy: Laemodonta (Bullapex) 
cubensis (Pfeiffer, 1854). 

Description: Shell to 9 mm long, oval-conic, 
solid, sometimes hirsute. Umbilicus present. 
Spire moderately high, sculptured with more 
or less marked spiral cords. Body whorl 70- 
75% shell length, sometimes truncate at 
base, with same sculpture as spire. Aperture 
about 70% length of body whorl, oval-elon- 



WESTERN ATLANTIC ELLOBIIDAE 



205 



gate, narrow; inner lip with three subequal 
teeth, one oblique columellar tooth and two 
parietal teeth; outer lip thickened, with one to 
three teeth about same size as parietal teeth. 
Protoconch smooth, globose, prominent. 

Remarks: Philippi (1846: 98), following the 
description of his Auricula striata, noted, 
'Taemodonta striata Adams (ubi?). Bronn 
placed under this name this species from 
Sandwich Islands [Hawaii]." The name Lae- 
modonta appeared as a nomen nudum in a 
sales catalogue of shells prepared by Bronn 
(1847, fide Sykes, 1894), who had sent the 
shells to Philippi. Although Laemodonta Phil- 
ippi, 1846, was introduced in synonymy, this 
name must be accepted as valid according 
to the ICZN, Article 11, (cO- Thiele (1931) and 
Zilch (1959) used Laemodonta and since 
1961 the name has been universally ac- 
cepted (Clench, 1964; Franc, 1968; Abbott, 
1974; Hubendick, 1978; Kay, 1979). 

The names Laimodonta and Laemodonta 
have been confused in many instances, the 
second being taken wrongly for a misspelling 
of the first. Laimodonta (Nuttall MS) H. & A. 
Adams, 1853, was introduced for a group of 
shells different from those assigned to Lae- 
modonta Philippi. Often credit was given er- 
roneously to Nuttall for the introduction of 
Laimodonta. It appears, however, that Nuttall 
never published the name (Sykes, 1894). 
Nevill (1879) considered "Laimodonta Nut- 
tall" [= emendation of Laemodonta Philippi] 
and Laimodonta H. & A. Adams to be differ- 
ent taxa and Ancey (1887) introduced Al- 
lochroa to replace H. & A. Adams' suppos- 
edly preoccupied name. Sykes (1894), 
apparently unaware of Ancey's introduction, 
also stated that Laimodonta H. & A. Adams 
was preoccupied, not by Philippi's (1846) or 
by Bronn's (1847) names, which he consid- 
ered undescribed, but by Lalmodon Gray, 
1841, a genus of birds. Sykes proposed the 
new name Enterodonta. Lalmodon Gray, 
1841, cannot be considered a homonym of 
Laimodonta or of Laemodonta. According to 
the ICZN, Art. 32 (a), in spite of the fact that 
Philippi (1846) misspelled Bronn's name, his 
spelling is to be considered the correct orig- 
inal spelling. Laimodonta (Nuttall MS) H. & A. 
Adams, although not a homonym of Philippi's 
name, has been abandoned in favor of Al- 
lochroa in important malacological works 
(Thiele, 1931; Zilch, 1959; Franc, 1968; Kay, 
1979). A permanent solution to this problem 
would be the placement of Laimodonta "Nut- 



tall" H. & A. Adams on the Official List of 
Rejected Names in Zoology. 

Sykes (1 894) and Hubendick (1 956) in their 
monographs on Laemodonta preferred the 
name Plecotrema H. & A. Adams to Philippi's 
name. Sykes recorded in his synonymy Lira- 
tor Beck, which he felt had not been properly 
introduced. The name LIrator, indeed, was 
used by Beck (1837) for an undescribed 
Melampus (LIrator) multlsulcatus from Opara 
Island. Pfeiffer (1856a, 1876) tentatively iden- 
tified Beck's species with Laemodonta striata 
Philippi [= Pedlpes octanfracta Jonas] and 
Hubendick (1956) accepted Pfeiffer's opinion 
without query. Because only circumstantial 
evidence connects Beck's names to a recog- 
nized species, however, one must conclude 
that both LIrator and Melampus (LIrator) mul- 
tlsulcatus are nomina nuda. 

Hubendick (1956; 111) stated that Aguayo 
& Jaume (1947) had given "strong reasons 
for maintaining Plecotrema as the valid name 
of the genus." In fact, what Aguayo & Jaume 
(1947; No. 132) had stated was, "in the im- 
possibility of deciding about the priority of 
Laemodonta [Philippi] 1847 [sic] over Laimo- 
donta [Bronn] 1847, and about the validity of 
LIrator [Beck], we have decided to use the 
genus Plecotrema [H. & A. Adams] as many 
modern authors do." Later Hubendick (1978) 
used Laemodonta Philippi and relegated Ple- 
cotrema to synonymy. As stated above, Lae- 
modonta Philippi is now universally ac- 
cepted. 

The genus Laemodonta has been assigned 
erroneously to the subfamily Pedipedinae on 
the basis of the shell. Although described as 
"fairly uniform" (Hubendick, 1 956; 1 1 0) or as 
a "convenient group" (Sykes, 1894: 241), the 
name Laemodonta is used now for a mixture 
of genera. Examination of the radula of "Lae- 
modonta" punctlgera H. & A. Adams from 
Malaysia has a very wide, rounded meso- 
cone, typical of the Cassldula group, and that 
species will be assigned to another genus 
pending more research. H. & A. Adams 
(1853: 120) had noted that Plecotrema [= 
Laemodonta] was "a genus of small shells 
allied to Cassldula." 

The present study of Laemodonta cuben- 
sls leads me to include this West Indian spe- 
cies within the Pythiinae on the basis of the 
radula and the reproductive and the nervous 
systems. Although preserved material of the 
type species was not available for anatomical 
comparisons, the remarkable resemblance of 
shell morphology, especially apertural denti- 



206 



MARTINS 



tion, of the West Indian species to Laemo- 
donta octanfracta (Fig. 3!) has led nne to con- 
clude that they are congeneric. If further 
anatomical studies indicate the necessity of 
taxonomic separation, the name Bullapex 
Haas is available for Laemodonta cubensis. 

I concur with Hubendick (1956) that the 
subgenus Bullapex Haas cannot be justified 
on the basis of shell characters alone. The 
true umbilicus of the West Indian species is 
often reduced to an umbilical depression, 
similar to the pseudoumbilicus mentioned by 
Haas (1950: 199) for Laemodonta clausa H. & 
A. Adams, 1853 [= Laemodonta octanfracta 
(Jonas)]. According to Hubendick (1 956: 1 1 4) 
the inflated apex can be explained as an eco- 
logically influenced character and as such is 
unreliable. The apex (protoconch) of Laemo- 
donta octanfracta, although not so prominent 
as that of Laemodonta cubensis, appears to 
be somewhat inflated (Fig. 92). 

According to Sykes (1894) and Hubendick 
(1 956) the genus Laemodonta appeared in the 
Eocene. These earlier species, unlike those 
recorded from the Miocene, are smoother and 
more similar to the West Indian Laemodonta 
cubensis. The Miocene species have the 
heavy sculpture of the Indo-Pacific group. 
Hubendick concluded that the West Indian 
species and the Indo-Pacific group probably 
had common ancestors in the Tethys Sea. 

Habitat: Because most of the data available 
to me pertain to Laemodonta cubensis, de- 
scription of the soft parts and comments on 
the habitat are presented under that species. 

Range: Hubendick (1956) noted the discon- 
tinuous distribution of Laemodonta. Most of 
the representatives are from the western 
Indo-Pacific, with one species in the West 
Indies and Bermuda. The genus is not repre- 
sented in the Recent fauna of the Mediterra- 
nean or Eastern Atlantic. 



Laemodonta cubensis (Pfeiffer, 1 854) 
Figs. 85-87, 89, 90, 93-101 

Plecotrema cubensis Pfeiffer, 1854b: 153 
[Cárdenas, Cuba; location of type un- 
known]; Pfeiffer, 1856a: 107; Pfeiffer 
1876: 348; Arango y Molina, 1880: 60 
Crosse, 1890: 259; Kobelt, 1900: 236 
Peile, 1926: 88; Aguayo & Jaume, 1947 
132; Hubendick, 1956: 111, text. fig. 1A, 
pi. 23, fig. 7 [distribution]. 



Plecotrema cúbense Pfeiffer. Sykes, 1895: 
245; Pilsbry, 1900b: 504, pi. 62, fig. 11. 

Laemodonta cubensis (Pfeiffer). Thiele, 1931 : 
464; Morrison, 1951b: 9; Morrison, 1958: 
1 1 8-1 24 [habitat]; Abbott, 1 974: 333, fig. 
4101; Emerson & Jacobson, 1976: 190, 
pi. 26, fig. 20; Rehder, 1981: 650, fig. 
222; Jensen & Clark, 1986: 458, figured. 

Laemodonta (Bullapex) cubensis (Pfeiffer). 
Haas, 1950: 199, pi. 22, figs. 6-8; Zilch, 
1959: 69, fig. 225; Clench, 1964: 123, pi. 
79 [taxonomy, distribution]; Vokes & 
Vokes, 1983: 60, pi. 31, fig. 18. 



Description: Shell (Figs. 85-87, 89, 90) to 3.5 
mm long, oval, somewhat solid, pale yellow 
to light brown, hirsute. Narrow umbilicus or 
umbilical depression present. Spire moder- 
ately high, whorls as many as six and one- 
fourth, weakly convex, with two incised spiral 
lines near suture; first whorls of teleoconch 
with fine, compact spiral striae, crossed by 
very fine, somewhat irregular growth lines. 
Body whorl about 70% shell length, with in- 
cised spiral lines. Aperture oval; inner lip with 
three evenly spaced teeth; columellar tooth 
oblique toward base, moderately strong; an- 
terior parietal tooth smallest, oblique poste- 
riorly; outer lip sharp, with two conspicuous 
teeth, sometimes with one or two much 
smaller tubercles posteriorly. Partition of in- 
ner whorls occupying about three-quarters of 
body whorl (Fig. 86). Protoconch whitish, 
smooth, inflated, oblique or perpendicular to 
columellar axis of teleoconch (Figs. 89, 90). 

Animal whitish, translucent; tentacles long, 
thin, subcylindric, translucent; foot entire, 
rounded posteriorly. Palliai cavity long; kid- 
ney long and thin; mantle gland curved, tu- 
bular, empties near vaginal opening. 

Radula (Figs. 93-97) having formula 
[24 + (7 + 7) + 1 + (7 + 7) + 24] x 1 00. Central 
tooth at about same plane as lateral teeth; 
base triangular, weakly emarginate anteriorly, 
with lateral prominences at mid-length; 
length of crown about half that of crown of 
lateral teeth, unicuspid; mesocone some- 
what sharp. Lateral teeth seven to ten; base 
weakly bent medially at posterior third, with 
lateral and medial prominences, the latter 
anteriormost; crown about half the length of 
the base, unicuspid, cuneiform. Transitional 
teeth five to nine; base similar to that of lat- 
eral teeth; crown bicuspid; endocone some- 
what shorter and weaker than mesocone. 
Marginal teeth 21 to 24; base becoming 



WESTERN ATLANTIC ELLOBIIDAE 



207 




FIGS. 85-92. Laemodonta, Ovatella. (85) L. cubensis (Pfeiffer), West Summerland Key, Florida, si 2.9 mm. 
(86) L. cubensis, Grassy Key, Florida, si 3.2 mm. (87) L. cubensis, Crawl Key, Florida, si 0.84 mm. (88) O. 
aequalis (Lowe), Sao Miguel, Azores, si 9.3 mm. (89) L. cubensis, lateral view of spire and protoconch. 
Grassy Key, Florida. (90) L. cubensis, top view of spire and protoconch, Grassy Key, Florida. (91) O. 
aequalis, top view of spire and protoconch, Sao Miguel, Azores. (92) L. octanfracta (Jonas), top view of spire 
and protoconch, Hawaii. Scale 1 mm. 



shorter and wider than that of lateral teeth, 
developing lateral basal cusp covered by 
next tooth; crovun tricuspid; endocone, me- 
socone and ectocone sharp, becoming 
subequal, with mesocone somewhat longer 
and stronger. 
Digestive system with salivary glands small, 



attaching posteriorly to esophagus through 
large area. Stomach (Fig. 98) tripartite; ante- 
rior portion corresponding to cardiac region, 
thin, dilated; mid-portion very muscular, with 
muscle also covering pyloric region; gastric 
caecum somewhat thin, not muscular, receiv- 
ing dilated, pouch-like posterior diverticulum 



208 



MARTINS 




FIGS. 93-96. Laemodonta cubensis, radular teeth, Grassy Key, Florida, si 3.5 mm. Scale 50 цт. 



IL 2L 11L IT 




FIG. 97. Laemodonta cubensis, radula. Grassy 
Key, Florida. Scale 10 |дт. 

anteriorly, at boundary with mid-region. Di- 
gestive gland with two subequal lobes. 

Reproductive system (Fig. 99) with ovotes- 
tis between lobes of digestive gland; seminal 
vesicle of hermaphroditic duct convoluted at 
mid-length; palliai gonoduct hermaphroditic 
to the vaginal aperture; anterior mucous 
gland and prostate gland cover entire length 
of spermoviduct; bursa duct about same 
length as spermoviduct and empties just 
posterior to vaginal opening; bursa spherical. 
Penis short, thin; vas deferens adhering to 
penis; penial retractor about as long as penis, 
Inserting on floor of palliai cavity. 

Nervous system (Fig. 100) with cerebral 
commissure short, about half width of cere- 




— -_ca 



FIG. 98. Laemodonta cubensis, stomach, Ber- 
muda. Scale 1 mm. 

bral ganglion; right cerebropedal and cere- 
bropleural connectives two-thirds length of 
left ones; left and right connectives of vis- 



WESTERN ATLANTIC ELLOBIIDAE 



209 



/T: 



-.^■', '. 



-Ot 




FIG. 99. Laemodonta cubensis, reproductive sys- 
tem, Hungry Bay, Bermuda. A-C, transverse sec- 
tions and tlneir locations. Scale 1 mm. 



pfvc Pfq piprc pig epic 




FIG. 100. Laemodonta cubensis, central nervous 
system. Hungry Bay, Bermuda. Scale 1 mm. 



cera! nerve ring equal; pleuroparietal connec- 
tives very short; parietovisceral connectives 
very long, the right one longer; visceral gan- 
glion beneath tentacle retractor muscle. 

Remarks: Laemodonta cubensis is the only 
representative of the genus in the Atlantic. All 
other species live in the Indo-Pacific region. 
The West Indian species is somewhat iso- 
lated conchologically, owing to its thinner, 
much less sculptured shell. Kobelt (1900) and 



Thiele (1 931 ) were not sure whether this spe- 
cies should even belong to this genus. As 
stated in the remarks under the genus, this 
species is included in Laemodonta because 
of the great similarity of its apertural morphol- 
ogy to that of the type species, Laemodonta 
striata (Philippi, 1846) [= Laemodonta octan- 
fracta (Jonas, 1845)]. The description of the 
radula of Plecotrema clausa H. & A. Adams, 
1853, a junior synonym of the type species, 
given by Odhner (1925) is very similar to that 
of Laemodonta cubensis except for the 
lesser number of teeth in a row in the latter. 

In the original description of Laemodonta 
cubensis, Pfeiffer (1854b; 153) characterized 
the shell as "hispidula" [slightly hairy], a fea- 
ture also noticed by Haas (1950). A pilose 
shell appears also in some Pacific species; 
Garrett (1872) noted that his Plecotrema hir- 
suta [= Laemodonta mollnifera (H. & A. Ad- 
ams)] had shorl, curved hairs. 

The presence of a palliai gland was some- 
what unexpected in Laemodonta. This organ 
of unknown function was first noticed by 
Plate (1897) in Phytia scarabeus (Linnaeus) 
and observed later in Carychium tridentatum 
(Risso) (Morton, 1955b), in Cassidula labrella 
(Deshayes) (Renault, 1966) and in Ovatella 
aequalis (Lowe) (Martins, personal observa- 
tion). Carychium lives inland, frequently in the 
mountains and, although preferring humid 
environments such as forest leaf litter, it is 
obviously a terrestrial species. Pythia is also 
considered a terrestrial ellobiid because it 
lives in the upper fringe of mangroves. Ova- 
tella aequalis lives just above the high-tide 
limit and Laemodonta at or just below the 
high-tide mark. Information is not available 
concerning the precise habitat of Cassidula 
labrella. Morton (1 955b, c) advanced the hy- 
pothesis that this was probably a case of par- 
allel evolution in response to some environ- 
mental parameter associated with terrestrial 
life. According to that same author, the pos- 
sible functions of the palliai gland range from 
help in forming egg cases to aid in keeping 
the body moist or secretion of bacteria-killing 
substances as a protective device while the 
animal is crawling. The presence of the palliai 
gland in two supposedly marine ellobiids de- 
mands a review of the hypotheses about the 
evolution and function of this organ. 

Laemodonta cubensis is very distinct from 
all other West Indian mollusks because of its 
hirsute, oval shell and its apertural dentition. 
Its protoconch and juveniles are very similarto 
the protoconch and hirsute juveniles of the 
Macaronesian and western European Ova- 



210 



MARTINS 




FIG. 101. Laemodonta cubensis, geographic dis- 
tribution. Open circle, locality from literature. 

tella aequalis (Lowe) (Figs. 89, 90). The 
strength of the palatal tooth of the aperture 
(Figs. 85, 88), the similarity of the radular teeth 
and the presence of the palliai gland (personal 
observations) also suggest a generic relation- 
ship between Laemodonta cubensis (Pfeiffer) 
and Ovatella aequalis (Lowe). 

Habitat: Laemodonta cubensis lives at or just 
below the high-tide mark, aggregating under 
half-burled porous rocks, rotting wood and 
leaves, and among the roots of propagules, 
together with Pedipes, Blauneria, Microtralia 
and Creedonia. It is common, along with Pe- 
dipes, in rocky areas, either under loose 
stones near the sediment, or in crevices in 
rock beds at about the high-tide mark. They 
prefer the part of loose stones that touches 
the sediment. 

Range: Bermuda; Captiva Island, on the 
western coast of Florida, south to the Florida 
Keys; Bahamas and Cuba, Jamaica south to 
Barbados; Mexico (Vokes & Vokes, 1983) 
(Fig. 101). 

Specimens Examined: FLORIDA: Third 
Ragged Key above Sand Key (USNM 
462737, 614608); Key Largo (MCZ 235475); 
N of Tavernier Key, Key Largo (A.M.); S of 
Ocean Drive, Plantation Key (A.M.); Indian 



Key Fill, N of Indian Key Channel (A.M.); In- 
dian Key (USNM 462893, 492557); Long Key 
(A.M.); Grassy Key (A.M.); Crawl Key (MCZ 
235469; A.M. Bonefish Key (ANSP 174978, 
219861; MCZ 110178; USNM 599365); 
Knight Key (A.M.); Bahia Honda Key (ANSP 
104109; MCZ 235472; USNM 492464); West 
Summerland Key (A.M.); Big Pine Key (ANSP 
1 041 1 0); Long Beach Drive and W end of Ko- 
hen Avenue, both Big Pine Key (A.M.); Little 
Torch Key (MCZ 235470); Big Torch Key 
(A.M.); Ramrod Key (MCZ 235471); Sugarloaf 
Key (ANSP 89559); Boca Chica Key (ANSP 
104111; USNM 270348); Garden Key, Dry 
Tortugas (USNM 492509, 492522); Seminole 
Point (ANSP 105438); Captiva Island (ANSP 
149410). BERMUDA (ANSP 62842, 293543; 
MCZ 24229; USNM 250298): Fairyland 
(ANSP 99078); N of Shelly Bay Beach (A.M.); 
North of Long Bird Bridge (A.M.); near St. 
Georges (ANSP 100821); Castle Harbour 
(ANSP 143321); Hungry Bay (A.M.); W of 
Somerset Bridge (A.M.); Ely's Harbour (A.M.); 
Mangrove Bay (A.M.). BAHAMAS ISLANDS: 
GRAND BAHAMA ISU\ND: Hepburn Town, 
Eight Mile Rock (ANSP 375427, 375455); Bell 
Channel, Lucaya (ANSP 370709); Dead Mans 
Reef [Sandy Bevan's Cay] (ANSP 371224); 
Bahama Beach Canal (ANSP 371802); Silver 
Cone Canal (ANSP 372886); North Riding 
Point (ANSP 375563); West End (ANSP 
368764); GREAT ABACO ISLAND: Mores Is- 
land (MCZ 116720); Sand Bank, Crossing 
Bay (MCZ 235474); S of Witch Point (MCZ 
235478); Wilson City (MCZ 235479); North 
Hawksbill Creek (ANSP 370566); ANDROS 
ISLAND (ANSP 151873): Morgan's Bluff 
(A.M.); South Mastic Point (A.M.); Mangrove 
Cay (USNM 590609, 614605); Solomon 
Pond, Mangrove Cay (USNM 614606); First 
island off Mintie Bar, SE of South Bight 
(USNM 590610, 614607); NEW PROVI- 
DENCE ISU\ND: Bar Point (A.M.); W of Rock 
Point (A.M.); W of Clifton Point (A.M.); E of 
Clifton Pier (A.M.); shore of Millars Road 
(A.M.); Malcolm Creek (A.M.); ELEUTHERA 
ISLAND: S of Rock Sound (MCZ 235473); 
EXUMA CAYS: NE coast. Hog Cay (MCZ 
235476), Western End, Hog Cay (MCZ 
235477). CUBA (ANSP 22544): near Habana 
(ANSP 130743); El Vedado, Habana (MCZ 
uncatalogued). JAMAICA: Falmouth (ANSP 
397272); Robin's Bay (USNM 442000). PU- 
ERTO RICO: San Juan (R.B.). VIRGIN IS- 
LANDS: ST. THOMAS (USNM 6427). 
LESSER ANTILLES: BARBADOS: oft Laza- 
reto (USNM 502107). 



WESTERN ATLANTIC ELLOBIIDAE 



211 



Subfamily Pedipedlnae 
Fischer & Crosse, 1 880 

Pedipedinae Fischer & Crosse, 1880: 5. 

Description: Shell to 1 1 mm long, globose 
to elongate. Spire low to high, with as many 
as six and one-half whorls. Body whorl 80- 
90% of shell length. Aperture broad to nar- 
row; columellar teeth one or two; parietal 
teeth one or two; outer lip smooth, with one 
strong tooth or with internal axial, ribbed cal- 
losity (Pseudomelampus). Inner whorls re- 
sorbed except in Pedipes and Creedonia. 

Animal whitish; foot transversely divided 
(except in Microtralia), posteriorly tapered, tip 
rounded. Mantle skirt broad, fused posteh- 
orly. Palliai cavity not occupying entire body 
whorl; kidney white, long to broadly triangu- 
lar; pneumostomal glands white and anterior 
to kidney; anal gill well developed; mantle or- 
gan lacking. 

Radula having very variable formula. Cen- 
tral tooth slightly posterior to lateral teeth, 
unicuspid or tricuspid. Lateral teeth bicuspid. 
Transition to marginal teeth gradual. Marginal 
teeth with as many as five cusps. 

Digestive system with mandible broadly 
rectangular, composed of numerous longitu- 
dinal fibers. Salivary glands white, small, fusi- 
form. Digestive gland of two roughly equal 
lobes; anterior lobe empties into crop 
through wide anterior diverticulum, just be- 
fore crop enters stomach; posterior lobe 
empties into gastric caecum through poste- 
rior diverticulum. Stomach tripartite, middle 
section very muscular and with a caecum. 

Reproductive system with hermaphroditic 
duct not convoluted (except in Marinula s.S.), 
posteriorly dilated; anterior mucous gland 
and prostate gland extending over proximal 
half of spermoviduct; bursa duct emptying 
just posterior to female opening, at which vas 
deferens separates from vagina (except in 
Pseudomelampus and Leuconopsis). Penis 
thick, usually with more or less developed 
diverticulum, simple in Microtraiia; vas defe- 
rens free, enters penis apically; penial retrac- 
tor short, attached to columellar muscle or to 
floor of palliai cavity. 

Nervous system with cerebral ganglia well 
developed; cerebropedal connectives about 
as long as cerebropleural connectives; pleu- 
roparietal connectives and parietovisceral 
connectives very short, somewhat longer in 
Leuconopsis. 



Remarl<s: Fischer & Crosse (1880) created 
the subfamily Pedipedinae for Pedipes, the 
only ellobiid genus then known to retain its 
inner whorls. On the basis of radular charac- 
ters Odhner (1 925) added to the subfamily the 
genera Marinuia and Plecotrema [= Laemo- 
donta], Thiele (1931) included Pseudomelam- 
pus and Leuconopsis and Morton (1955c) 
added Rangitotoa [= Microtralia]. In 1 959 Zilch 
transferred Rangitotoa to the Melampinae and 
added Apodosis, which I consider a junior 
synonym of Leuconopsis. Abbott (1 974) listed 
Microtralia within the Cassidulinae and erro- 
neously considered Ovatella [sensu Myoso- 
tella] to belong to the Pedipedinae. My anal- 
ysis of nervous and reproductive systems 
leads to the inclusion of Microtralia in the Pe- 
dipedinae and to the removal of Laemodonta, 
Ovatella and Myosotella to the Pythiinae. A 
new genus, Creedonia, is here created upon 
the basis of the conchological and radular 
characters of Creedonia succinea (Pfeiffer, 
1854), formerly placed in the genus Marinula. 
Creedonia does not resorb the inner whorls, 
its central and lateral radular teeth are broad 
with only a few in a row and the marginal teeth 
have several endocones but lack ectocones. 
The radulae in those species of Marinula stud- 
ied have numerous, very long, narrow lateral 
teeth and marginal teeth with one endocone 
and several ectocones (Figs. 163-168). 

The subfamily is best characterized ana- 
tomically. The nervous and reproductive sys- 
tems have very consistent patterns, whereas 
the shell and radula vary somewhat. The 
short connectives of the visceral ring cause 
the concentration of those ganglia. This fea- 
ture also exists in the Melampinae and sets 
these two groups apart from the remaining 
subfamilies, which have long visceral ring 
connectives. The cerebral ganglia in the Pe- 
dipedinae are proportionally much larger 
than the other ganglia. The reproductive sys- 
tem differs from that of the Melampinae by its 
acinose ovotestis, its unconvoluted seminal 
vesicle of the hermaphroditic duct, its longer 
spermoviduct, its junction of the bursa duct 
near the female opening, and its elaborate 
penial complex, sometimes with a long diver- 
ticulum. From the other three subfamilies it 
differs by its elaborate penial complex with 
free anterior vas deferens, and by its prostate 
and anterior mucous glands that cover only 
the posterior half of the spermoviduct. 

The genus Leuconopsis deviates in some 
anatomical features from the typical Pedipe- 
dinae pattern in that its visceral nerve ring is 



212 



MARTINS 



longer and its reproductive system is semi- 
diaulic, the vas deferens and vagina sepa- 
rating from the common spermoviduct half- 
way along the pallia! gonoduct. The visceral 
nerve ring is not so long as that of any of the 
species belonging to the Pythiinae and Ello- 
biinae here studied and does not justify per 
se the exclusion of Leuconopsis from the 
Pedipedinae. The organization of the palliai 
gonoducts of Leuconopsis resembles that of 
Pseudomelampus (Martins, personal obser- 
vation) in that the vas deferens separates 
from the spermoviduct some distance before 
reaching the female opening, giving rise to a 
long, nonglandular vagina. The arrangement 
of the reproductive organs in Leuconopsis is, 
then, v\/ithin the range of variation seen within 
the Pedipedinae. Shell and radular charac- 
ters also justify the inclusion of Leuconopsis 
within the Pedipedinae. 

The Pedipedinae are represented in the 
West Indies by Pedipes, Creedonia, Leu- 
conopsis and Microtralia, all of which are 
readily distinguishable on conchological 
characters. Pedipes is globose, generally 
heavily sculptured, with two strong columel- 
lar teeth, a large oblique, posteriorly placed 
parietal tooth and a readily visible callous 
tooth on the outer lip, opposite the parietal 
tooth. Creedonia has an apertural configura- 
tion similar to that of Pedipes, but lacks the 
tooth on the outer lip and has an elongate, 
smooth and very thin shell. The minute Leu- 
conopsis has an elongate, thick shell that 
lacks the parietal and teeth on the outer lip. 
The shell of Microtraiia is very thin and trans- 
parent and has a long, narrow aperture with 
the outer lip smooth inside, one columellar 
tooth and two anteriorly placed parietal teeth, 
of which the anterior is the strongest. 

IHabitat: The Pedipedinae are a group of 
small species that live at or below the high- 
tide zone (Morton, 1955c; Martins, 1980), 
sometimes reaching the low intertidal area 
(Spencer, 1979). They live mainly in crevices 
and under half-buried rocks. Some (Cree- 
donia, IVIicrotralia) live in the soft, black sed- 
iment of the high-tide region of mangroves, 
or in the spaces around the underground root 
system of propagules and adult plants. 

Range: Worldwide, warm and temperate ar- 
eas. In the Western Atlantic the Pedipedinae 
occur in Bermuda and from south Florida to 
the West Indies, Central America south to 



Brazil, Ascension Island and Tristan da 
Cunha (Connolly, 1915). 

Genus Pedipes Scopoli, 1777 

Pedipes Scopoli, 1777: 392. Type species by 
subsequent designation of Gray (1 847a): 
Pedipes afra (Gmelin, 1791) [= Pedipes 
pedipes (Bruguière, 1789)]. 

Carassa Gistel, 1847 [1850]: 555 [substitute 
name for Pedipes Scopoli]. 

Description: Shell to 6 mm long, globose, 
solid to fragile, white to dark brown. Spire 
low, with as many as five rapidly expanding 
convex whorls, with incised spiral grooves. 
Body whorl averaging 87% of shell length. 
Aperture about 70% length of body whorl, 
ovate, widely rounded at base; exposed por- 
tion of columella flat and depressed, with two 
strong columellar teeth, posterior one stron- 
ger; parietal tooth strongest, oblique; outer 
lip sharp, smooth or with thick, elevated 
tooth opposite parietal tooth. Inner whorls 
not resorbed. Protoconch with apex involute 
in first teleoconch whorls, smooth, translu- 
cent, yellowish to brown. 

Animal grayish; tentacles long, pointed, 
with transparent base, blackish toward tip. 

Radula with 150 to 450 teeth in a row; first 
30 to 40 rows without marginal teeth. Central 
tooth at same level as lateral teeth; base 
long, slightly indentate anteriorly, wide and 
angular in first quarter, longitudinally de- 
pressed in the middle, becoming narrower 
posteriorly; crown as wide as base, falciform, 
with long mesocone. Lateral teeth as narrow 
as but longer than central tooth, laterally 
compressed; base irregularly thickened lon- 
gitudinally; crown falciform, laterally com- 
pressed; mesocone long; endocone half 
length of mesocone, pointed. Transitional 
teeth four to eight, with base becoming 
shorter, crown becoming wider; two or three 
endocones. Marginal teeth cteniform, with 
very thin, short base; wide rounded crown, 
connected to base by long neck bent up- 
wards; as many as six short endocones; me- 
socone somewhat stronger than endocones. 

Visceral mass coiled. Digestive gland yel- 
lowish; posterior diverticulum becoming 
pouch-tike before entering anterior portion of 
gastric caecum. Stomach tripartite; anterior 
thin-walled, pouch-like section that receives 
crop on left and empties into intestine on 
right; middle thick-walled, very muscular giz- 
zard; posterior membranous, extensible cae- 



WESTERN ATLANTIC ELLOBIIDAE 



213 



cum that receives posterior diverticulum at 
junction with gizzard. Ovotestis acinose, em- 
bedded in posterior lobe of digestive gland; 
hermaphroditic duct dilated along most of its 
length; bursa spherical. Penis unevenly thick- 
ened, convoluted in middle. Cerebral com- 
missure long; connectives of visceral ring 
very short; penial nerve originating from right 
middle labial nerve. 

Remarks: The name Pedipes was first used 
by Adanson (1 757), who gave a very detailed 
and accurate description of a species from 
Senegal later described as Pedipes pedipes 
and accepted as the type species of the ge- 
nus. Adanson, a contemporary of Linnaeus, 
derived the generic group name from the 
French word, pietin, meaning pedestrian, 
which refers to the way in which the animal 
progresses, first advancing the anterior half 
of the transversely divided foot, then moving 
the posterior half, seemingly advancing by 
steps. Adanson's work (1757) antedates the 
starting point of zoological nomenclature and 
therefore he is not credited with introducing 
Pedipes. The first post-Linnaean use of Pe- 
dipes was that of Scopoli (1 777), who briefly 
characterized Pedipes "Adanson" as having 
the shell aperture diversely dentate. The only 
known species, not mentioned by Scopoli, 
was Adanson's African "pietin," introduced 
by Bruguière (1 789) as Bulimus pedipes. He- 
lix afra Gmelin, 1791 [= Pedipes pedipes 
(Bruguière, 1789)] was designated type spe- 
cies of Pedipes by Gray (1847a). 

Férussac (1821) used Pedipes in a re- 
stricted sense but Blainville (1824), using 
the sharp outer lip as the major diagnostic 
character, included a heterogeneous as- 
semblage, i.e., Conovulus [= Melampus] and 
the opisthobranch genus Tornatella. Lowe 
(1832), following Lamarck (1822) and Menke 
(1828), treated Pedipes as a genus of the 
family "Plicacea" and tried to prove that the 
animal was a pectinibranch. After Crosse & 
Fischer (1879) noticed that Pedipes was the 
only known ellobiid that did not resorb the 
inner whorls of the shell, the genus could be 
separated easily from otherwise conchologi- 
cally similar groups, e.g., Marinula. In this 
study the genus Creedonia too was found not 
to resorb the inner whorls. The radula of Pe- 
dipes too is unique because the posterior- 
most 30 to 40 rows lack marginal teeth (Fig. 
140). 

The genus Pedipes is represented in the 
Western Atlantic by two species. The larger 



(6 mm) Pedipes mirabilis has a thick, globose, 
generally heavily sculptured shell; the visible 
part of the protoconch consists of hardly 
more than one whorl and has a sinuous, 
elongate apertural lip. The smaller (3.5 mm), 
more elongate Pedipes ovalis has a thicker- 
shelled, rock-dwelling form and a thinner- 
shelled, mangrove-inhabiting form. The pro- 
toconchs of both forms are identical, with 
more than one and one-third whorls visible 
and with round, not sinuous, apertural lips. 

Habitat: The genus Pedipes lives in man- 
groves near the sea, in which animals are 
abundant under fallen leaves and branches 
below the high-tide mark. They also live 
along open rocky shores in crevices and un- 
der stones frequently covered by waves at 
high tide. 

Range: Worldwide, warm temperate to trop- 
ical regions. In the Western Atlantic they oc- 
cur in Bermuda, southern Florida to Texas, 
the West Indies and Central America south to 
Brazil and Ascension Island. 

Pedipes mirabilis (Mühlfeld, 1816) 
Figs. 102-106, 108-110, 112-120 

Turbo mirabilis Mühlfeld, 1816: 8, pi. 2, figs. 
13a, b [Locality unknown, herein desig- 
nated Cabo Rojo lighthouse, Puerto 
Rico; type specimens presumed lost, 
fide Clench (1964); neotype herein des- 
ignated MCZ 188476a (Fig. 102)]. 

Pedipes mirabilis (Mühlfeld). Beck, 1837: 
105; Pfeiffer, 1856a: 70; Pfeiffer 1876: 
333; Mörch, 1878: 5; Nevill, 1879: 221; 
Pilsbry, 1900b: 503; Dali & Simpson, 
1901: 369, pl. 53, fig. 8; Aguayo & 
Jaume, 1947: 218; Morrison, 1951b: 9; 
Morrison, 1958: 121 [ecology]; Nowell- 
Usticke, 1959; 88; Warmke & Abbott, 
1961; 152, pl. 28, fig. j; Rios, 1970: 138; 
Morris, 1973: 274, pl. 74, fig. 12; Rios, 
1975: 159, pl. 48, fig. 767; Rosewater, 
1975: 23; Emerson & Jacobson, 1976: 
189, pl. 21, fig. 20; Rehder, 1981: 648, 
fig. 234; Vokes & Vokes, 1 983: 60, pl. 31 , 
flg. 16 Ouvenile; not positively this spe- 
cies]; Mahieu, 1984: 314 pp; Jensen & 
Clark, 1986: 458, figured. 

Pedipes quadridens Pfeiffer, 1840: 251 
[Cuba; location of type unknown]; С. В. 
Adams, 1849: 41, 42; С. В. Adams, 
1851: 186; Pfeiffer, 1854b: 148; Shuttle- 
worth, 1854b: 102; H. & A. Adams, 



214 



MARTINS 



1855b: 149: Shuttleworth, 1858: 73: 
Poey, 1866: 394. 

Pedipes globulosas С. В. Adams, 1845: 12 
[Jamaica: lectotype by Clench & Tumer 
(1950), MCZ 177347 (Fig. 103)]; Clench 
& Turner, 1950: 288, pi. 49, fig. 9. 

Pedipes globulsus "Petit" Pfeiffer, 1856a: 
70 [Haiti; type from Cuming's collection, 
not seen at BMNH]; Pfeiffer, 1876: 333. 
Non "Férussac" H. & A. Adams, 1854 
(nomen nudum). 

Pedipes mirabilis (Mühlfeld) [in part] Arango y 
Molina, 1880: 60; Dali, 1889: 92, pi. 47 
fig. 17; Crosse, 1890: 259; Kobelt, 1900 
255, pi. 24, figs. 19, 20; Maury, 1922: 54 
С. W. Johnson, 1934: 159; M. Smith, 
1937: 145, pi. 55, fig. 8 [probably Pe- 
dipes ovalis; pi. 67, fig. 17 is Pedipes 
ovalis]; M. Smith, 1951: [same illustra- 
tions as in first edition, 1937]; Clench, 
1964: 119, pi. 76, figs. 1, 3, pi. 77 [fig. 2 
is lectotype of Pedipes ovalis С В. Ad- 
ams; systematics, distribution]; An- 
drews, 1971: 144, text fig. [figure prob- 
ably is of Pedipes ovalis]; Abbott, 1974: 
333, fig. 4096 [in part]; Andrews, 1977: 
181, text fig. [figure probably is of Pe- 
dipes ovalis]. 

Pedipes mirabilis Megerle. Peile, 1926: 88. 

Description: Shell (Figs. 102-106, 108-110) 
to 6 mm long, globose, very solid, white 
to brown. Spire low, as many as five con- 
vex whorls, sculptured with incised spiral 
grooves and fine axial striae. Body whorl av- 
eraging 88% of shell length, with average of 
22 deeply incised spiral grooves. Sculpture 
as on spire; spiral grooves sometimes subdi- 
vided by fine spiral cords. Aperture about 
70% of length of body whorl, widely ovate, 
round to angular at base, sometimes with 
weak angle at shoulder; columella flat and 
weakly concave, with two strong, rounded, 
subequal teeth perpendicular to cotumellar 
axis; parietal tooth strongest, oblique and 
slightly curved anteriorly; outer lip wide and 
smooth in juveniles, thick and crenulated in 
adults owing to grooves of body whorl; op- 
posite parietal tooth one large tooth very 
weakly extends inside aperture. Protoconch 
with barely more than one whorl visible, ap- 
ertural lip sinuous (Figs. 108-110). 

Radula (Figs. 1 1 2-1 1 6) as in genus; formula 
[120 + (6 + 70) + 1 + (70 + 6) + 120] X 120. 

Stomach (Fig. 117) as in genus. 

Reproductive system (Fig. 118) with her- 
maphroditic duct with longitudinally dilated 



seminal vesicle; bursa duct longer than sper- 
moviduct and albumen gland conbined. Pos- 
terior half of penis thicker than anterior por- 
tion. 

Nervous system (Fig. 119): left cerebrope- 
dal and cerebropleural connectives longer 
than right ones; left parietovisceral connec- 
tive twice length of right one; visceral gan- 
glion largest of five in visceral ring; left pleural 
and left parietal ganglia smaller than right 
counterparts. 

Remarks: In spite of the great variability 
shown by West Indian Pedipes, recent au- 
thors consider all of the named forms con- 
specific. According to Clench (1964) variabil- 
ity in Pedipes is a result of colonization 
strategy. Most colonies might have begun 
from one individual or from one cluster of 
eggs. Clench based this observation upon 
the meager representation of Pedipes in mu- 
seum collections, because he clearly stated 
(p. 1 1 8), "there is nothing in the literature . . . 
concerning their life history." The colonies 
are not so rare as Clench implied. Pedipes 
species are among the most common West 
Indian ellobiids just below the high-tide mark, 
at least in mangroves (Martins, personal ob- 
servation). 

Pedipes mirabilis prefers piles of loose 
rocks around the high-tide mark. The shell is 
always thick, deeply grooved, with the aper- 
ture constricted in adults by a thick outer lip 
tooth. The body whorl of gerontic animals 
shows asymmetric growth. The name 
"quadridens'' of Pfeiffer (1840) reflects the 
change in apertural aspect with age, and the 
names "gf/obu/osus" of С В. Adams (1845) 
and "globulus'' of Pfeiffer (1856a) refer to the 
allometric growth of this species. 

In 1849 С В. Adams cautiously introduced 
Pedipes ovalis, calling attention to its strong 
affinity with Pfeiffer's Pedipes quadridens. Al- 
though the latter species is here considered a 
junior synonym of Pedipes mirabilis, Pedipes 
ovalis is recognized here as a separate spe- 
cies on the basis of size, sculpture and pro- 
toconch. The thick-shelled, heavily toothed 
Pedipes ovalis that С В. Adams described 
from Jamaica rarely occurs in mangroves 
(Martins, personal observation), where the 
much thinner-shelled, smoother Pedipes tri- 
dens Pfeiffer [= Pedipes ovalis С В. Adams] 
abounds. Their similar protoconchs and the 
sizes suggest, however, that both rock- 
dwelling and mangrove-dwelling forms are 
expressions of the same species. The simi- 



WESTERN ATLANTIC ELLOBIIDAE 



215 




FIGS. 102-111. Pedipes. (102) P. mirabilis (Mühlfeld), neotype (MCZ 188476a), Cabo Rojo lighthouse, 
Puerto Rico, si 4.7 mtn. (103) P. globulosus C. B. Adams, lectotype (MCZ 177347), Jamaica, si 4.6 mm. 
(104) P. mirabilis, Puerto Cabello, Venezuela, si 6.0 mm. (105) P. mirabilis, Rio Grande do Norte, Brazil 
(ANSP 300179), si 3.8 mm. (106) P. mirabilis, Morgan's Bluff, Andres Island, Bahamas, si 5.0 mm. (107) P. 
pedipes (Bruguière), Senegal (AMNH 22590), si 7.7 mm. (108) P. mirabilis, lateral view of spire and proto- 
conch, Maravén, Venezuela. (110) P. mirabilis, top view of spire and protoconch, Shelly Bay, Hamilton, 
Bermuda. (Ill) P. pedipes, top view of spire and protoconch, Sâo Miguel, Azores. Scale 1 mm. 



larities of Pedipes ovalis with Pedipes mira- 
bilis should, then, be interpreted as adapta- 
tions for life in rocky environments. A more 
detailed comparison between these two spe- 
cies is presented under the remarks on Pe- 
dipes ovalis. 



Pedipes mirabilis is similar to the Eastern 
Atlantic Pedipes pedipes (Bruguière), mostly 
in the shape of the protoconch (Fig. 111). 
The Eastern Atlantic species, however, has a 
double outer lip tooth and a bifid, downward- 
curved parietal tooth (Fig. 107). 



216 



MARTINS 








FIGS. 112-115. Pedipes mirabilis, radular teeth. (112) Shelly Bay, Bermuda, si 2.3 mm. (113-115) El Palito, 
Venezuela, si 3.2 mm. Scale 50 \im. 



C1L9L 65L 75L80L1T2T 3T IM 




2M 3M 4M 38M 40M 81M 124M 




FIG. 116. Pedipes mirabilis, radula. El Palito, Ven- 
ezuela. Scale 10 |.im. 

H. & A. Adams (1854) listed a Pedipes 
globulus Férussac, which might be confused 
with the homonym introduced by Pfeiffer 




FIG. 117. Pedipes mirabilis, stomach, Bahamas. 
Scale 1 mm. 



WESTERN ATLANTIC ELLOBIIDAE 



217 




FIG. 118. Pedipes mirabilis, reproductive system, 
Clifton Pt., New Providence, Bahamas. A-C, trans- 
verse sections and their locations. Scale 1 mm. 




vg pfvc 



FIG. 119. Pedipes mirabilis, central nervous sys- 
tem, Clifton Pt., New Providence, Bahamas. Scale 
1 mm. 



(1856a) for a West Indian specimen. Such a 
name does not appear in Férussac (1821). 
The Adams brothers might have intended to 
refer to Pedipes ovulus, which Férussac 
(1 821 : 1 09) described as "longer than afra [= 




FIG. 120. Geographic distributions, Pedipes mira- 
bilis (circles) and Leuconopsis manningi (star). 
Open circle, locality from literature. 

Pedipes pedipes], smooth and shiny, v\/ithout 
tooth on the outer lip." Perhaps Férussac 
was dealing with a specimen of Marinula, 
which Connolly (1915) with doubt referred to 
Marinula xanthostoma H. & A. Adams. Pe- 
dipes globulus was described by Pfeiffer 
(1856a) using Petit's manuscript name in the 
Cuming collection, and it is considered syn- 
onymous with Pedipes mirabilis. The name 
Pedipes globulus "Férussac" H. & A. Adams 
should be considered a nomen nudum. 

A Pedipes, tentatively assigned to Pedipes 
mirabilis, was found in the Early Miocene 
Cantaure Formation in Venezuela (Gibson- 
Smith & Gibson-Smith, 1979). Recently 
(1985) the Gibson-Smiths described those 
fossils as Pedipes mirandus, which I consider 
a junior synonym of Pedipes ovalis (see the 
remarks for this species). 

Habitat: Pedipes mirabilis usually lives on 
rocky shores, often where wave action is 
strong. The animals aggregate in fairly large 
numbers under rocks at or just below the 
high-tide mark. 

Range: Bermuda; Florida, Texas; West In- 
dies, Central America, northern South Amer- 
ica to Sao Paulo, Brazil (Rios, 1975); Ascen- 
sion Island (Fig. 120). 

Specimens Examined: FLORIDA: Daytona 
(USNM 162346, 253173); Indian River 
(USNM 758222); Lake Worth (MCZ 205366; 



218 



MARTINS 



USNM 599349); Palm Beach Inlet (MCZ 
110215; USNM 543392); Boca Raton (ANSP 
219865); S Bayshore Dr., Miami (USNM 
701950); Biscayne Bay (MCZ 291105); Hau- 
lover Beach Park, Biscayne Bay (USNM 
809777). TEXAS: Port Aransas (MCZ 225522, 
229626); Mustang Island, Port Aransas (MCZ 
235614); South Padre Island (ANSP 319092; 
USNM 758649); Port O'Connor (USNM 
711183). BERMUDA (ANSP 48599, 62741; 
MCZ 9952, 24251, 167937); Flatts (USNM 
171948); Shelly Bay (MCZ 25523; A.M.); N of 
Long Bird Bridge (A.M.); W of Somerset 
Bridge (A.M.); Ireland Island (USNM 712378). 
BAHAMA ISIJ\NDS; GRAND BAHAMA IS- 
LAND; W of Eight Mile Rock (R.B.); Hepburn 
Town, Eight Mile Rock (ANSP 370410); Car- 
avel Beach, Freeport (ANSP 370228); Tama- 
rind Shipway, Lucaya (ANSP 370708); 
GREAT ABACO ISLAND: Wilson City (ANSP 
299513; USNM uncatalogued); Sweeting's 
Village (MCZ 24142); Sand Bank, Crossing 
Bay (MCZ 116721); Mores Island (MCZ 
116719); ANDROS ISLAND: Morgan's Bluff 
(A.M.); South Mastic Point (A.M.); Mangrove 
Cay (USNM 180462a); PARADISE ISLAND 
(A.M.); NEW PROVIDENCE ISLAND: Bar 
Point (A.M.); Delaport Point (A.M.); Rock 
Point (A.M.); Clifton Point (A.M.); E of Clifton 
Pier (A.M.); ROYAL ISLAND (MCZ 78360). 
CUBA: El Vedado (MCZ 167983); Matanzas 
Bay (ANSP 167481; MCZ 83308, 109334, 
167984); Peñas Altas (MCZ 127866); Playa 
de Bellamar (ANSP 222590, 345332); Ver- 
salles (MCZ 92075); Muelle de la Aduana, 
Matanzas (MCZ 188903); Chivera, Bahia de 
Santiago (MCZ 167985); Cayo Francés (MCZ 
167982); Guantánamo Bay (ANSP 313059). 
JAMAICA (ANSP 22565, 22570, 22572; MCZ 
117347, 117348, 185170; USNM 90459, 
94747): Montego Bay (USNM 441609); Rob- 
in's Bay (MCZ 167896; USNM 441978); 
Jack's Bay (MCZ 167895; USNM 441836); 
Manchioneal (USNM 492493); Port Morant 
(USNM 423674); Rock Fort (MCZ 167894; 
USNM 423792); Kingston (USNM 442594); 
Kingston Harbor (MCZ 314005); Palisadoes 
(USNM 442540); Mouth of Rio Cobre, Port 
Royal (USNM 426870); Hunt's Bay (USNM 
441675); Little River (USNM 492506). HAITI: 
St. Louis (MCZ 167899; USNM 439397); Port 
Salut (MCZ 167891; USNM 440000); Les 
Cayes (USNM 439780); Aquin (USNM 
367339, 440107); Baie Anglaise, near Aquin 
(USNM 439605); Saltrou (MCZ 167897, 
167898, 223892; USNM 439341); W of Me- 
tesignix (USNM 404730); Bizoton (USNM 



439843). DOMINICAN REPUBLIC: Santo Do- 
mingo (ANSP 60920; USNM 492507); Santa 
Bárbara de Samaná (ANSP 173412; MCZ 
57783); Cayo Chico, 4 km E of Santa Bárbara 
de Samaná (MCZ 57784). PUERTO RICO: Pi- 
ñones, W of Boca de Cangrejos (A.M.); Pu- 
erta de Tierra, San Juan (A.M.); Punta Arenas, 
N of Joyuda (A.M.); Cabo Rojo lighthouse 
(MCZ 188476, 188476a); Humacao (MCZ 
166297); Ensenada Honda, Culebra Island 
(USNM 159675). VIRGIN ISLANDS: ST. 
CROIX (USNM 621393, 706774): Christian- 
sted (MCZ 188477); ST. THOMAS (ANSP 
22569; USNM 119543); GUANA ISLAND: 
North Beach (MCZ 89245); ST. JOHN (ANSP 
22568). LESSER ANTILLES: ST. THOMAS 
(MCZ 294220); ST. KITTS (MCZ 167935) 
BARBUDA: Spanish Point (ANSP 353819) 
GUADELOUPE (ANSP 22566; MCZ 181419) 
MARTINIOUE (MCZ 167936, 294221; USNM 
612694); Pointe Pie, 2.5 km S of Ste. Anne 
(MCZ 248315); GRENADINES: Union, Admi- 
ralty Bay, Bequia Island (MCZ 216484); BAR- 
BADOS (MCZ 167900, 167939; USNM 
502106); TOBAGO: Buccoo Bay (ANSP 
188276); TRINIDAD (MCZ 90508): Toco 
(MCZ 62326). CARIBBEAN ISLANDS: CAY- 
MAN ISLANDS: Cayman Brae (MCZ 294222); 
ARUBA (USNM 663655). CURAÇAO: Port 
Marie & Daaibooi Baai (R.B.). COSTA RICA 
Pórtete (USNM 702836, 706405). PANAMA 
Toro Point, Fort Sherman (USNM 734066) 
Limon Bay, inside Toro Point (USNM 732870 
R.B.); Fort Randolph (USNM 759237). CO- 
LOMBIA: Sabanilla (MCZ 167890; USNM 
103468, 193615). VENEZUELA: Cayo Punta 
Brava (A.M.), Parque Nacional de Morrocoy, 
Tucacas (A.M.); El Palito (A.M.); Puerto Ca- 
bello (A.M.); Maravén, Borborata (A.M.). 
BRAZIL: Praia do Forte, Natal, Rio Grande do 
Norte (ANSP 300179). ATLANTIC ISLANDS: 
ASCENSION ISLAND (USNM 735717). 

Pedipes ovalis С В. Adams, 1849 
Figs. 121-148 

Pedipes ovalis C. B. Adams, 1849: 41 [Ja- 
maica; lectotype by Clench & Turner 
(1950) MCZ 177349 (Fig. 121)]; С В. Ad- 
ams, 1851: 186; Pfeiffer, 1854b: 148; H. 
& A. Adams 1855b: 249; Pfeiffer, 1856a: 
70; Pfeiffer, 1876: 333; Clench & Turner, 
1 950: 321 , pi. 1 41 , fig. 1 4 [lectotype fig- 
ured]; Morrison, 1951b: 9; Morrison, 
1958: 121 [ecology]; Morton, 1955c: 
127-168 [evolution]. 

Pedipes tridens Pfeiffer, 1854b: 148 [nomen 
nudum]. 



WESTERN ATLANTIC ELLOBIIDAE 



219 



Pedipes tridens Pfeiffer, 1855: 122 [Bermuda 
and Cárdenas, Cuba, herein restricted to 
Bermuda; lectotype herein selected 
BMNH 1967590 (Fig. 122)]; H. & A. Ad- 
ams, 1855b: 249; Pfeiffer, 1856a: 72; 
Pfeiffer, 1876: 333; Pilsbry, 1900b: 503, 
pl. 62, fig. 10; Peile, 1926: 88; Haas, 
1950: 198, pl. 22, fig. 4. 

Pedipes naticoides Stearns, 1869: 108, text 
fig. [Rocky Pt., Tampa Bay, Florida; ho- 
lotype USNM 37598 (Fig. 123)]; Pfeiffer, 
1876: 334; Dali, 1883: 323; Dali, 1885: 
279, pl. 18, fig. 17; Simpson, 1889: 69. 

Pedipes mirabilis (Mühlfeld) [in pari]. Arango 
y Molina, 1880: 60; Dali, 1889: 92, pl. 47 
fig. 17; Crosse, 1890: 259; Kobelt, 1900 
255, pl. 24, figs. 19, 20; Maury, 1922: 54 
C.W. Johnson, 1934: 159; M. Smith, 
1937: 145, pl. 55, fig. 8 [probably Pe- 
dipes ovalis; pl. 67, flg. 17 is Pedipes 
ovalis]; M. Smith, 1951: [same illustra- 
tions as in first edition, 1937]; Clench, 
1964: 119, pl. 76, figs. 1, 3, pl. 77 [fig. 2 
is lectotype of Pedipes ovalis C. B. 
Adams; systematics, distribution]; An- 
drews, 1971: 144, text fig. [figure prob- 
ably is of Pedipes ovalis]; Abbott, 1974: 
333, fig. 4096 [in part]; Andrews, 1977: 
181, text fig. [figure probably is of Pe- 
dipes ovalis]. Non Mühlfeld, 1816. 

Pedipes insularis Haas, 1950: 197, pl. 22, fig. 
3 [Lover's Lake, St. George's, Bermuda; 
holotype FMNH 30171 (not seen); para- 
type ANSP 212176 (Fig. 124)]. 

Pedipes mirabilis, forma ovalis C. B. Adams. 
Robertson, 1960: 22. 

Pedipes mirandas Gibson-Smith & Gibson- 
Smith, 1985: 88, fig. 1 [Early Miocene 
Cantaure Formation, Paraguaná Penin- 
sula, Venezuela; holotype NHMB No. H 
17113 (not seen)]. 

Description: Shell (Figs. 121-139) to 3.5 mm 
long, oval, solid to thin, yellow to dark brown; 
spire low, whorls four and one-half, convex, 
sculptured with incised spiral grooves; mi- 
crosculpture of grooves composed of very 
fine, irregular, compressed axial lamellae, 
sometimes crossed by spiral lines; ribs 
smoothish, sometimes with incised spiral 
lines; slightly matte appearance caused by 
fine growth lines crossing spiral ribs. Body 
whorl averaging 85% of shell length, with 15 
to 34 deeply incised spiral grooves. Aperture 
about 70% of length of body whorl, widely 
ovate to squarish, round to somewhat angu- 
late at base; columella flat and weakly con- 



cave, with two rounded teeth, the posterior 
one stronger, anterior one sometimes very 
weak; parietal tooth oblique, longest; outer 
lip somewhat angular posteriorly, frequently 
smooth in thin-shelled forms (Figs. 122-124, 
126-128); thick-shelled forms usually with 
strong, ridge-like tooth opposite parietal 
tooth, extending inside aperture (Figs. 121, 
125, 129, 132). Protoconch with more than 
one and one-third whorls visible, apertural lip 
round, not sinuous (Figs. 133-139). 

Radula (Figs. 140-144) as in genus; for- 
mula [75 + (5 + 50) + 1 + (50 + 5) + 75] x 120. 

Stomach (Fig. 145) as in genus. 

Reproductive system (Fig. 146) with her- 
maphroditic duct anteriorly dilated to form 
seminal vesicle; bursa duct shorter than sper- 
moviduct and albumen gland combined. An- 
terior half of penis thicker than posterior half. 

Nervous system (Fig. 147) with left cere- 
bropedal and cerebropleural connectives 
about twice length of right ones; left parieto- 
visceral connective about as long as right 
one; visceral ganglion largest of five in vis- 
ceral nerve ring; left pleural ganglion and left 
parietal ganglion three times larger than right 
counterparts. 

Remarks: Pedipes ovalis is very variable 
(Figs. 121-132). A stout, highly sculptured 
form could be confused with Pedipes mirabi- 
lis. In fact, С В. Adams (1849: 41) introduced 
his description of Pedipes ovalis with the 
words, ^^ Pedipes ovalis may be a variety of 
Pedipes quadridens Pfeiffer [= Pedipes mira- 
bilis (Mühlfeld)]." As С. В. Adams pointed 
out, it differs from Pedipes mirabilis by the 
smoothness of its body whorl and the less 
conspicuous tooth on the outer lip. The outer 
lip tooth in Pedipes ovalis is often ridge- 
shaped and it gradually diminishes into the 
aperture, whereas in Pedipes mirabilis this 
tooth is more tubercle-shaped. In Pedipes 
ovalis the anterior columellar tooth usually is 
weaker than the posterior one. The most 
consistent character differentiating these 
species, however, is the protoconch, which 
in Pedipes ovalis is larger and has a rounded, 
not sinuous, lip. 

Smoother, thin-shelled examples were 
named Pedipes tridens by Pfeiffer (1 855), Pe- 
dipes naticoides by Stearns (1869) and Pe- 
dipes insularis by Haas (1950) (Figs. 
122-124). This form differs from the typical 
thick-shelled form in the greater number of 
grooves on the body whorl and in the wider, 
somewhat quadrangular aperture that some- 



220 



MARTINS 




FIGS. 121-132. Pedipes ovalis С. В. Adams. (121) Lectotype (MCZ 177349), Jamaica, si 3.1 mm. (122) 
P. trídens Pfeiffer, lectotype (BMNH 1967590), Bermuda, si 3.4 mm. (123) P. naticoides Stearns, Inolotype 
(USNM 37598), Tampa Bay, Florida, sl 2.4 mm. (124) P. insularis Haas, paratype (ANSP 212176), Lover's 
Lake, Bermuda, sl 2.4 mm. (125) Clifton Ft., New Providence, Bahamas, sl 2.3 mm. (126) Shore of Millars 
Road, New Providence, Bahamas, sl 2.3 mm. (127) Crawl Key, Florida, sl 2.3 mm. (128) Plantation Key, 
Florida, sl 3.5 mm. (129) Punta Arenas, Puerto Rico, sl 2.8 mm. (130) Isla Mujeres, Yucatán, Mexico (R.B.), 
sl 2.6 mm. (131) Fort Sherman, Panama (USNM 620532), sl 3.3 mm. (132) Puerto Cabello, Venezuela, sl 
3.0 mm. 



times has a weak tooth inside the outer lip. 
The snnoothness of the body whorl is very 
evident in the thin-shelled form although 
there is much variability and overlap with the 
thick-shelled form. Owing to unifying fea- 
tures, such as the identical protoconch, and 
the continuation and gradual disappearance 
of the outer lip tooth into the aperture, how- 
ever, the thin-shelled form should be consid- 
ered conspecific with Pedipes ovalis. 



The thick-shelled forms of Pedipes ovalis 
live mostly in rocky habitats, whereas the 
thin-shelled forms are predominantly man- 
grove-dwellers. In Punta Arenas, Puerto 
Rico, both species of Pedipes live in an area 
in which mangrove trees cover the rocky 
shore. At this site Pedipes ovalis showed a 
wide range of thickness and corresponding 
variability in the conspicuousness of the 
tooth on the outer lip (Fig. 129). In the Florida 



WESTERN ATLANTIC ELLOBIIDAE 



221 




FIGS. 133-139. Pedipes ovalis. (133) Juvenile, Crawl Key, Florida, sl 0.45 mm. (134) Juvenile, Crawl Key, 
Florida, sl 0.55 mm. (135) Juvenile, Crawl Key, Florida, sl 0.55 mm. (136) Lateral view of spire and proto- 
conch, Clifton Pt., New Providence, Bahamas. (137) Top view of spire and protoconch, Clifton Pt., New 
Providence, Bahamas. (138) Top view of spire and protoconch. Punta Arenas, N of Joyuda, Puerto Rico. 
(139) Top view of spire and protoconch. Isla Mujeres, Yucatán, Mexico. Scale 1 mm. 



Keys, in v\/hich I failed to collect Pedipes mi- 
rabilis and from which I could not confirm any 
museum records referring to that species, 
Pedipes ovalis in most mangroves appears 
as Pfeiffer's Pedipes tridens or Stearns' Pe- 



dipes naticoides. In rocky areas, however, 
the sculpture and shape approach those of 
Pedipes mirabilis. 

Anatomical research yielded some small 
differences in the reproductive and nervous 



222 



MARTINS 




FIGS. 140-143. Pedipes ovalis, radular teeth. (140) Whole radula, Ely's Harbour, Bermuda, si 3.1 mm. (141) 
Morgan's Bluff, Andros Island, Bahamas, si 2.7 mm. (142, 143) Ely's Harbour, Bermuda, si 2.7 mm. Scale, 
Fig. 140, 1 mm; all others, 50 цт. 



WESTERN ATLANTIC ELLOBIIDAE 

С 1L2L3L 34L 38L46L47L1T2T 3T 4T 



223 




FIG. 144. Pedipes ovalis, radula, Ely's Harbour, '**'■ 

Bermuda. Scale 10 цт. 



/" I 



er 




ca 



FIG. 145. Pedipes ovalis, stomach, Florida. Scale 
1 mm. 



systems, and counts of radular teeth are 
lower in Pedipes ovalis. On that basis, but 
mostly on the bases of the protoconch, the 
generally more disparate sizes of the col- 
umellar teeth, the shape of the outer lip tooth 
and the maximal size, Pedipes ovalis is con- 
sidered distinct from Pedipes mirabilis. The 
resemblance of the two species can be inter- 
preted as convergence due to adaptation to 
the same environmental pressures of the 
rocky shore. The gradation from the thick- 
shelled, rock-dwelling forms to the thin- 
shelled, mangrove-dwelling populations, to- 
gether with the retention of the same pattern 
of protoconch and shape of the tooth on the 




FIG. 146. Pedipes ovalis, reproductive system, 
Florida. Scale 1 mm. 



ad 




.pyi 


ra 


.car 


prvc 


.mb 




~pd 





vg 




FIG. 147. Pedipes ovalis, central nervous system, 
Florida. Scale 1 mm. 



outer lip, amply justify the inclusion of Pe- 
dipes tridens, Pedipes naticoides and Pe- 
dipes insularis as junior synonyms of Pedipes 
ovalis. 

As stated under the remarks on the previ- 
ous species, Gibson-Smith & Gibson-Smith 
(1985) described a Pedipes mirandus from 
the Early Miocene Cantaure Formation of 
Venezuela. The authors did not mention the 
shape of the protoconch, the decisive char- 
acter for the separation of the Western Atlan- 
tic species. Judging from the accentuated 
difference in size of the columellar teeth, 
however, I consider Pedipes mirandus a jun- 



224 



MARTINS 




FIG. 148. Pedipes ovalis, geographic distribution. 

lor synonym of Pedipes ovalis. The specimen 
of the latter species that I collected in Vene- 
zuela (Fig. 132) closely resembles the illustra- 
tion of the holotype of Pedipes mirandus 
(Gibson-Smith & Gibson-Smith, 1985: 88, 
fig. 1). 

Habitat: Pedipes ovalis often occurs with Pe- 
dipes mirabilis under rocks and in crevices at 
or just below the high-tide mark. The thinner- 
shelled forms are very common in man- 
groves under leaves, twigs and rocks at or 
just below high-tide mark. The juveniles ven- 
ture farther into the intertidal zone than do 
any other West Indian ellobiid. 

Range: Bermuda; Florida; West Indies; Mex- 
ico south to Panama and Venezuela (Fig. 
148). 

Specimens Examined: FLORIDA: Waveland 
(USNM 123531); Miami (ANSP 320358; 
USNM 159439, 330934); Ocean Beach 
(USNM 270714); Third Ragged Key above 
Sand Key (USNM 462738); Key Largo (USNM 
597459); Tavernier Key (USNM 492504); 
Plantation Key (MCZ 188973, 291000, 
291003); Ocean Dr., Plantation Key (A.M.); 
Upper Matecumbe Key (USNM 492492); In- 
dian Key (MCZ 167889; USNM 492520); In- 
dian Key Fill, N of Indian Key Channel (A.M.); 



Lignumvitae Key (ANSP 156683); Lower 
Matecumbe Key (MCZ 167893; USNM 
492495); Long Key (ANSP 219860; A.M.): 
Grassy Key (ANSP 89560, 397279; MCZ 
188970; A.M.); Crawl Key (MCZ 188972, 
289998, 289999; A.M.); Bonefish Key (ANSP 
227991); Knight Key (MCZ 188971); Bahia 
Honda (ANSP 104115; MCZ 188969); West 
Summerland Key (A.M.); Big Pine Key (ANSP 
1 041 1 4, 227999; MCZ 291 1 04); W end of Ko- 
hen Avenue and Long Beach Drive, both on 
Big Pine Key (A.M.); Little Torch Key (MCZ 
188974, 291108); Big Torch Key (ANSP 
104112); Ramrod Key (MCZ 188975; USNM 
599368); Sugarloaf Key (ANSP 89561, 
104113; MCZ 188478); Boca Chica Key 
(MCZ 167892; USNM 270349); Key West 
(ANSP 22563; USNM 36017, 492494); SW 
channel, Dry Tortugas (USNM 492505); Gar- 
den Key, Dry Tortugas (USNM 590210); Fla- 
mingo Key (ANSP 29431 3); Cape Sable (MCZ 
291103); Seminole Point (ANSP 105432); 
Sanibel Island (MCZ 84103); Tarpon Bay, 
Sanibel Island (MCZ 84339); Captiva Island 
(ANSP 149408); Starvation Key (ANSP 
130059); Palmetto (A.M.); Mullet Key (USNM 
652408, 653109; A.M.); Shell Key (USNM 
466287); Tampa Bay (MCZ 239222; USNM 
37598a); Anclote Key (ANSP 22564). MEX- 
ICO: Isla Cancún, Quintana Roo (ANSP 
285534). BERMUDA: (ANSP 48597, 48600, 
48601, 48602; MCZ 9952a, 74809, 314027; 
USNM 6523, 94438, 492496): Fairyland 
(ANSP 99077, 1 1 1 096; USNM 208071 ); Flatts 
(USNM 171963); Shelly Bay (MCZ 225523); 
Old Road, Shelly Bay (A.M.); Coney Island 
(A.M.); N of Long Bird Bridge (A.M.); Nonsuch 
Island (MCZ 248274); Lover's Lake (ANSP 
212176); Cooper's Island (ANSP 131648); 
Hungry Bay (A.M.); W of Somerset Bridge 
(A.M.); Ely's Harbour (A.M.); Mangrove Bay 
(A.M.). BAHAMA ISLANDS: BIMINI (ANSP 
325624): East Well, East Bimini (ANSP 
326449); N. end of Pigeon Cay, Bimini La- 
goon (ANSP 326022; USNM 656173); S end 
of Pigeon Cay (ANSP 326017); Cavelle Pond, 
South Bimini (ANSP 325548); Tokas Cay 
(ANSP 325831); GRAND BAHAMA ISLAND: 
W of Eight Mile Rock (R.B.); Running Mon 
Canal (ANSP 369780); North Hawksbill Creek 
(ANSP 370569); Dead Mans Reef [Sandy Be- 
van's Cay] (ANSP 371226, 371285); Sweet- 
ings Cay (ANSP 374312); Riding Point (ANSP 
371521); West End (ANSP 368763, 371933); 
GREAT ABACO ISU\ND: West Point (ANSP 
299478); Gorling Cay (ANSP 299549); AN- 
DROS ISLAND: Morgan's Bluff (A.M.); South 



WESTERN ATUXNTIC ELLOBIIDAE 



225 



Mastic Point (A.M.); Danlin Bay (USNM 
180671); Mangrove Cay (ANSP 325639; 
USNM 180462); First island off Mintie Bar, SE 
end of South Bight (USNM 271784); NEW 
PROVIDENCE ISLAND: Delaporte Point 
(A.M.); E of Clifton Pier (A.M.); Clifton Bluff 
(MCZ 205367); Clifton Point (A.M.); Millars 
Road (A.M.); Malcolm Creek (A.M.); ROYAL 
ISLAND (MCZ 78360, 167901; USNM 
468120); ELEUTHERA ISLAND: Governor's 
Harbor (MCZ 167995); EXUMA CAYS: Hog 
Cay (MCZ 225560, 225561); CAY SAL BANK: 
Salt Lagoon, Cay Sal (USNM 513429). CUBA 
(USNM 492498): Dimas (USNM 614603); Ha- 
bana (ANSP 130744); Las Villas, Caibarién 
(USNM 608763). JAMAICA (MCZ 177348a, 
177349, 177350, 185170a; USNM 90460, 
94748): Falmouth (ANSP 397266); Robin's 
Bay (MCZ 167896a; USNM 441978a); Jack's 
Bay (MCZ 167895a; USNM 441836a); Port 
Morant (USNM 423674a); Palisadoes (USNM 
442540a). HAITI: St. Louis (USNM 439397a); 
Port Salut (USNM 440000a); Bizoton (USNM 
439843a). PUERTO RICO: San Juan (R.B.); 
Punta Arenas, N of Joyuda (A.M.); Cabo Rojo 
lighthouse (MCZ 188476b). VIRGIN IS- 
LANDS: ST. CROIX (USNM 706775); ST. 
THOMAS (ANSP 22562). LESSER ANTILLES: 
ST. KITTS (MCZ 167935a; USNM 492491); 
GRENADA: Caliveny Harbor (ANSP 296716); 
ST. MARTIN (MCZ 250474). MEXICO: Isla 
Mujeres, Quintana Roo (R.B.). BELIZE: Twin 
Cays (USNM 841329); Drowned Cays (ANSP 
284811). PANAMA: Devil's Beach, Fort Sher- 
man (USNM 620532). CARIBBEAN IS- 
LANDS: ST. ANDREWS ISLAND (ANSP 
155415). VENEZUELA: Puerto Cabello (A.M.). 

Genus Creedonia new genus 

Type species: Creedonia succinea (Pfeif- 
fer, 1854). 

Description: Shell to 3.8 mm long, oval-elon- 
gate, fragile. Spire moderately high, trun- 
cated, with rounded apex; as many as four 
smooth, weakly convex whorls. Body whorl 
about 80% of shell length. Aperture oval- 
elongate, about 70% of body whorl length, 
posteriorly acuminate, rounded at base; col- 
umella somewhat oblique and twisted; col- 
umellar teeth two, posterior one stronger; pa- 
rietal tooth a little stronger than posterior 
coiumellar tooth; outer lip sharp, smooth. In- 
ner whorls not resorbed. Protoconch large, 
smooth, with nuclear whorls covered by first 
whorls of teleoconch. 



Radula with about 45 teeth in a row; central 
tooth wide, with triangular base, small, uni- 
cuspid crown; lateral teeth with strong en- 
docone; transitional teeth with two en- 
docones; marginal teeth with as many as five 
endocones. 

Animal whitish; tentacles long, pointed. 
Visceral mass coiled. Pallia! cavity elongate; 
kidney long, thin. Hermaphroditic duct some- 
what dilated in the middle; penis with long 
diverticulum. Nervous system with long cere- 
bral commissure. 

Remarl<s: The genus Creedonia is created 
for Creedonia succinea (Pfeiffer) upon the ba- 
sis of shell, radular and anatomical charac- 
ters. This new genus is closely related to Pe- 
dipes and Marinula, and the type species was 
formerly included in one or the other genus. 
Creedonia, like Pedipes, does not resorb its 
inner whorls and, like Marinula, has a smooth 
shell and a smooth outer lip. The three gen- 
era characteristically have two coiumellar 
teeth and one strong parietal tooth. 

As stated above, Creedonia succinea for- 
merly was considered to belong to the genus 
Marinula. Only twice have some species of 
Marinula been assigned tentatively to new 
genera. Swainson (1855) introduced the ge- 
nus Cremnobates in which he included his 
three species Cremnobates cornea, Cremno- 
bates parva and Cremnobates solida, all from 
Tasmania. Hedley & Suter (1910) noted that 
Cremnobates cornea is a junior synonym of 
Ophicardelus australis (Ouoy & Gaimard, 
1832) and that Cremnobates solida is con- 
specific with Marinula patula (Lowe, 1832). 
They therefore selected Cremnobates pan/a 
(Fig. 156) as type of the genus. Connolly 
(1915) considered Cremnobates parva allied 
to Marinula xanthostoma H. & A. Adams, 
1855. Iredale (1936; 328) proposed Mar- 
ipythia for Marinula xanthostoma H. & A. Ad- 
ams on the basis of Connolly's opinion that 
that species "could not be classed under 
Marinula." This is a misinterpretation of the 
statements of Connolly (191 5: 118) who, after 
tracing the tortuous history of Marinula xan- 
thostoma, concluded, "the typical form of 
xanthostoma is on the extreme borderland of 
Marinula," but added that intermediate forms 
occurred in different localities, a fact making 
the connection with Marinula less doubtful. 

Research on the anatomy of a Mahnula cf. 
xanthostoma H. & A. Adams, conchologically 
related to Cremnobates parva, revealed a re- 
productive system similar to that of Pedipes. 



226 



MARTINS 



The reproductive system of Marinula pepita 
King, 1832, the type species of the genus, 
differs considerably from that of the Adams' 
species, leading to the conclusion that they 
are at least subgenerically separated. The 
similarity of the radular teeth of Marinula 
pepita to those of Marinula filholi (Hutton, 
1878) (Figs. 163-168), conchologically allied 
to Marinula xanthostoma, casts doubt upon 
their generic separation. Because I lacked 
an opportunity to examine the anatomy of 
Cremnobates parva to assess its relationship 
to Marinula xanthostoma, I think a decision 
about the synonymy of the names proposed 
by Swainson and Iredale is unwarranted. 

The genus Marinula has been confused with 
Ovatella [Pythiinae] on the basis of the appar- 
ent similarity of the dentition of the inner lip. H. 
& A. Adams (1855b) created the subgenus 
Monica to include the Mediterranean Monica 
firminii (Payraudeau, 1 826) [= Ovatella firminif], 
and the Madeiran Monica aequalis (Lowe, 
1 832) [= Ovatella aequalis] and Monica gracilis 
(Lowe) [= Ovatella aequalis]. The shells of 
Marinula are easily separated from those of 
Ovatella on the basis of their apertural teeth. 
Marinula, Pedipes and Creedonia all have two 
conspicuous columellar teeth, whereas Ova- 
tella has only one columellar tooth. The pari- 
etal tooth of Marinula is the strongest of the 
three inner lip teeth, whereas in Ovatella the 
anterior parietal tooth is the strongest (Fig. 
88). Connolly (1915) added as a diagnostic 
character of the genus the absence of teeth 
on the outer lip, but the Eastern Pacific 
Marinula concinna (C. B. Adams, 1852) and 
Marinula brevispira (Pilsbry, 1920) have a 
thick, ridge-like tooth opposite the parietal 
tooth. Anatomical research on these species 
is needed to ascertain their phylogenetic re- 
lationships, however. 

Marinula is known from the Indo-Pacific 
and it is well represented along the Pacific 
coasts of Central and South America; it has 
been reported from the South Atlantic Islands 
and from South Africa as well (Connolly, 
1915). 

The new genus Creedonia differs from 
Marinula by having a thinner, smaller shell 
that is less than half the size of that of any 
species included in Marinula, with the possi- 
ble exception of Marinula mandroni Velain, 
1877, which Connolly (1915) suspected to 
have been named after a young specimen of 
Marinula velaini Connolly, 1915. In Creedonia 
the columella is twisted and oblique, instead 
of flat and straight, and the anterior columel- 
lar tooth is always conspicuous, whereas in 



Marinula it is very small (Figs. 155-157). The 
spire in Creedonia is more elevated, the apex 
is truncate and perforated (Fig. 158) instead 
of acuminate and obliterated as in Marinula 
(Fig. 159). As stated above, Creedonia ani- 
mals do not resorb the inner whorls of the 
shell (Fig. 153), whereas those of Marinula 
species do. 

The radula of Creedonia succinea differs 
from that of Marinula in its broad central and 
lateral teeth and in the very small number of 
teeth in a row (Table 3, Appendix). The mar- 
ginal teeth have several endocones but no 
ectocones, whereas in the Neozealandic 
Marinula filholi (Hutton) and in Marinula pe- 
pita King there are one or two endocones and 
several ectocones (Figs. 163-168). 

The genus Creedonia is named in honor of 
the Rev. Joseph Dennis Creedon, Pastor of 
Christ the King Church, Kingston, Rhode Is- 
land, as an expression of my gratitude for his 
support in this research and for his invaluable 
friendship. 

Creedonia succinea (Pfeiffer, 1 854) 
Figs. 149-154, 158, 160-162, 169-173 

Leuconia succinea Pfeiffer, 1854b: 156 [Cár- 
denas, Cuba; location of type unknown]; 
Pfeiffer, 1856a; 157; Pfeiffer, 1876; 370; 
Arango y Molina, 1880; 61; Crosse, 
1890; 260; H. & A. Adams, 1855b: 248. 

Pedipes elongatus Dall, 1885; 279, pi. 18, fig. 
4 [Marco, Florida; lectotype herein se- 
lected USNM 859012 (Fig. 149); five 
paralectotypes USNM 37599]; Dalí, 
1889; 92, pi. 47, fig. 4; Simpson, 1889: 
60; Kobelt, 1900; 258, pi. 24, figs. 17, 18; 
Maury, 1922; 54; С W. Johnson, 1934: 
159; M. Smith, 1937, pi. 67, fig. 4 [pi. 
from Dall (1885)]; Emerson & Jacobson, 
1976; 190, pi. 26, fig. 21. 

Mar/na/a succ/nea (Pfeiffer). Morrison, 1951b: 
9; Morrison, 1958: 118-124 [habitat]; 
Abbott, 1974; 333, fig. 4100 [not fig. 
4108]; Vokes & Vokes, 1983: 60, pi. 31, 
fig. 17. 

Description: Shell (Figs. 149-154, 158) to 
3.8 mm long, oval-elongate, fragile, shiny, 
translucent, pale yellow to golden brown. 
Spire truncate, with as many as four and 
one-half weakly convex, apparently smooth 
whorls; very fine spiral lines visible under 
high magnification, crossed by weak, irregu- 
larly spaced growth lines; spiral depression 
just below suture. Body whorl about 80% of 
shell length, smooth. Aperture oval-elongate, 



WESTERN ATLANTIC ELLOBIIDAE 



227 




FIGS. 149-159. Creedonia, Marínala. (149) Pedipes? elongatus Dali, lectotype (USNM 859012), Marco, 
Florida, sl 3.9 mm. (150) С succinea (Pfeiffer), Crawl Key, Florida, sl 2.3 mm. (151) С succinea, Big Pine 
Key, Florida, sl 3.3 mm. (152) С succinea, Isla Mujeres, Yucatán, Mexico (R.B.), sl 4.3 mm. (153) C. 
succinea, Isla Mujeres, Yucatán, Mexico (R.B.), sl 3.3 mm. (154) С succinea, lateral view of spire and 
protoconch. Crawl Key, Florida. (155) /W. pepita King, syntype (BMNH 1968882), Chiloe Island, Chile, sl 10.1 
mm. (156) M. parva (Swainson), New Zealand (USNM 98181), sl 6.4 mm. (157) M. fillioli (Hutton), New 
Zealand, (USNM 681303), sl 5.4 mm. (158) С succinea, top view of spire and protoconch. Crawl Key, 
Florida. (159) M. fillioli, top view of spire and protoconch. New Zealand (USNM 681303). Scale 1 mm. 



about 70% of length of body whorl, round at 
base; columella somewhat oblique, twisted; 
columellar teeth two, oblique toward base; 



anterior columellar tooth conspicuous, pos- 
terior columellar tooth twice the size of ante- 
rior; parietal tooth lamelliform, as large as or 



228 



MARTINS 



somewhat larger than posterior columellar 
tooth; outer lip sharp, smooth. Inner whorls 
not resorbed (Fig. 153). Protoconch large, 
smooth, whitish, translucent; nuclear whorls 
enveloped by first whorl of teleoconch, leav- 
ing pit in apex of shell (Figs. 154, 158). 

Radula (Figs. 160-162, 169) with formula 
[12 + (2 + 12) + 1 + (12 + 2) + 12] X 80. Base 
of central tooth as wide as that of lateral 
teeth, rhomboidal, with anterior end much 
shorter than posterior, rounded; crown as 
wide as posterior end of base; mesocone 
small, triangular, with rounded tip; no ecto- 
cones. Lateral teeth eight to 12; base qua- 
drangular, medially bent at half-length; crown 
as wide as posterior end of base, triangular, 
with rounded tip; endocone about half the 
length of mesocone, strong, weakly pointed. 
Transitional teeth two, with base wider than 
that of lateral teeth, with two subequal en- 
docones. Marginal teeth 12 to 14; base be- 
comes shorter and wider; mesocone be- 
comes smaller as teeth approach lateral 
edge of radula; first marginal tooth with three 
subequal endocones; fourth endocone ap- 
pears on fourth marginal tooth, fifth en- 
docone on tenth marginal tooth. 

Animal whitish, translucent; tentacles mod- 
erately long, somewhat pointed, translucent, 
with bulbous base. Foot transversely divided. 
Palliai cavity elongate; kidney broad, triangu- 
lar, white. 

Digestive system with salivary glands 
small, fusiform. Stomach globose, very mus- 
cular; gastric caecum conspicuous, membra- 
nous (Fig. 170). Digestive gland bilobed; 
anterior lobe covers most of stomach and 
empties into pouch-like posterior crop 
through dilated anterior diverticulum; intes- 
tine very dilated as it comes off the stomach. 

Reproductive system (Fig. 171) with ovo- 
testis acinose, embedded in posterior lobe 
of digestive gland; hermaphroditic duct with 
irregularly dilated seminal vesicle; fertilization 
pouch bilobed, very conspicuous; albumen 
gland large, triangular; posterior mucous 
gland weakly convoluted; anterior mucous 
gland and prostate gland cover posterior half 
of spermoviduct. Bursa duct thick, shorter 
than spermoviduct; bursa elongate. Penis 
with several pouch-like dilations, with very 
long diverticulum wrapped around esopha- 
gus and salivary glands; short penial retractor 
attaches to columellar muscle; vas deferens 
short, free. 

Nervous system (Fig. 172) with cerebral 
commissure just shorter than width of cere- 



bral ganglion; left cerebropedal and cere- 
bropleural connectives shorter than right 
ones; pedal commissure very conspicuous; 
cerebral ganglia large, elongate laterally; left 
pleural ganglion about one-fourth size of right 
one; left parietal ganglion about one-tenth 
size of right one; visceral ganglion largest of 
visceral ring, somewhat smaller than pedal 
ganglia. 

Remarks: Creedonia succinea was originally 
assigned by Pfeiffer (1854b) to the genus 
Leuconia Gray [= Auhculinella Tausch, 1886]. 
The species appeared in the literature under 
this name until placed by Morrison (1951b) in 
the genus Marinula King, 1832, in which it 
has remained until now. 

Dall (1885) apparently was not aware of 
Pfeiffer's species when he introduced Pe- 
dipes elongatus for specimens from Marco, 
Florida. Creedonia succinea is one of the few 
species of ellobiids that shows little morpho- 
logical variation. It cannot be confused with 
any other West Indian species. The superfi- 
cial similarity to the Mediterranean Ovatella 
was already pointed out in the remarks under 
the genus Creedonia. In Creedonia the col- 
umellar tooth is double and the parietal tooth 
is the strongest or at least as strong as the 
posterior columellar tooth. In Ovatella there is 
only one columellar tooth and the first pari- 
etal tooth is the strongest. The same applies 
to the introduced Myosotella myosotis, with 
the difference that in this species the poste- 
rior parietal tooth is either absent or weaker 
than the anterior parietal tooth. The spire of 
Creedonia succinea is truncate and the pro- 
toconch gives it a mucronate appearance. 
The elongate, smooth, translucent shell, with 
flat whorls, separates Creedonia succinea 
from the thin-shelled form of Pedipes ovalis 
with which it occurs. Microtralia and Blaune- 
ria also occur with Creedonia; the former 
differs from Creedonia in having a narrow 
aperture with much smaller inner lip teeth 
and a very short spire. Blauneria is sinistral, 
has a high spire and is white and transpar- 
ent, whereas Creedonia is straw-colored to 
brown. 

Connolly (1915: 105), in his monograph on 
the genus Marinula, apparently was not ac- 
quainted with Pfeiffer's species. He men- 
tioned ''Pythia abbreviatus Beck," criticizing 
Pfeiffer's (1 856a) questionable attribution of it 
to Marinula in these terms: "whatever may be 
its true genus, as the shell is said to come 
from the Antilles it is quite unlikely to be a 



WESTERN ATLANTIC ELLOBIIDAE 



229 




FIGS. 160-168. Creedonia, Marinula, radular teeth. (160-162) С. succinea, Long Key, Florida, si 3.0 mm. 
(163) M. filholi, New Zealand, si 5.4 mm. (164) M. filholi, New Zealand, si 5.5 mm. (165) M. filholi, New 
Zealand, si 5.4 mm. (166-168) M. tristanensis Connally [= M. pepita King], Gough Island (BMNH), si 10.8 
mm. Scale 50 ).im. 



230 MARTINS 

С 1L 2L 11L 12L IM 2M 3M 15M 16M 




piprc pipe cpc cplc 



cg cc bg 



FIG. 169. Creedonia succinea, radula, Long Key, pc,^ r-~^^ 
Florida. Scale 10 um. ~~-~~, "í''^- 




FIG. 170. Creedonia succinea, stomach, Crawl 
Key, Florida. Scale 1 mm. 




FIG. 171. Creedonia succinea, reproductive sys- 
tem, Crawl Key, Florida, sl 3.3 mm. A-C, trans- 
verse sections and their locations. Scale 1 mm. 



Marinula.'' Beck (1837: 105) had listed, with- 
out description, a "Pythia abbreviatus'' from 
the West Indies, placing the name after 
Pythia aequalis (Lowe, 1832) [= Ovatella ae- 




FIG. 1 72. Creedonia succinea, central nervous sys- 
tem, Crawl Key, Florida, sl 3.0 mm. Scale 1 mm. 

quails] and Pythia patulus, which is question- 
ably referred by Connolly (1915) to Marlnula 
xanthostonna H. & A. Adams. Pfeiffer (1856a) 
did not see Beck's specimens but tentative- 
ly assigned Pythia abbrevlatus Beck to 
Marlnula, no doubt on the basis that Beck 
listed it between two species that Pfeiffer 
considered to be Marlnula. The only other 
species in the Western Atlantic that at first 
glance could be confused with Creedonia 
succinea is Myosotella myosotis, which 
does not live in the West Indies. In spite of 
the fact that some circumstancial evidence 
seems to indicate that Beck's name refers to 
Creedonia succinea, Pythia abbrevlatus Beck 
must remain a nomen nudum. 

Habitat: Individuals of Creedonia succinea 
live about the high-tide mark, the juveniles 
venturing a short distance into the interlidal 
zone. They live within the sediment, some- 
times 10 to 15 cm deep, and they occur fre- 
quently under half-buried rotting wood or 
rocks and on the roots of mangrove propa- 
gules, together with Pedlpes, MIcrotralla and 
Blaunerla. 

Range: Georgia ?, Florida Keys and the Ba- 
hama Islands south to Cuba and Jamaica; 
Mexico (Fig. 173). The USNM record from 
Isle of Hope, Georgia, collected by Hubricht, 
is so distant from the normal range that it 
could be explained better as the result of ac- 
cidental transportation by currents. 

Specimens Examined: GEORGIA: Isle of 
Hope (USNM 663054). FLORIDA: S of Ocean 
Drive, Plantation Key (A.M.); Lignumvitae Key 



WESTERN ATLANTIC ELLOBIIDAE 



231 



(ANSP 156694); Long Key (A.M.); Grassy Key 
(A.M.); Crawl Key (A.M.); Big Pine Key (ANSP 
293553); Long Beach Drive and W of Kohen 
Avenue, both Big Pine Key (A.M.); Newfound 
Harbor (USNM 272639); Big Torch Key 
(ANSP 1 041 05); Sugarloaf Key (ANSP 89566, 
104104); Ramrod Key (MCZ 235471a); Boca 
Chica Key (USNM 590597); Key West (USNM 
450693); Seminole Point (ANSP 105410); 
Marco (ANSP 22578; USNM 37599, 859012); 
Captiva Island (ANSP 149409); Mullet Key 
(USNM 652409; A.M.); Mullet Key Bayway 
(USNM 653110). BAHAMA ISLANDS: 
GRAND BAHAMA ISU\ND: South Hawksbill 
Creek (ANSP 371809); ANDROS ISLAND: 
South Mastic Point (A.M.). CUBA: Matanzas 
(MCZ 131760). JAMAICA: Kingston (USNM 
442584). MEXICO: N end of Ascension Bay, 
Quintana Roo (USNM 736105); Isla Mujeres, 
Quintana Roo (R.B.). 

Genus Microtralia Dali, 1894 

Microtralia Dali, 1894: 117. Type species by 
monotypy: Auricula ? {Microtralia) mi- 
núscula (Dali, 1889) [= Leuconia occi- 
dentalis Pfeiffer, 1854]. 

Rangitotoa Powell, 1933: 148. Type species 
by monotypy: Rangitotoa insularis Pow- 
ell, 1933. 

Description: Shell to 3.8 mm long, subcylin- 
dric, fragile, translucent white. Spire low to 
moderately high, with as many as seven 
weakly convex whorls. Body whorl 80% of 
shell length. Aperture narrow, about 90% of 
body whorl length; inner lip with small, ob- 
lique columellar tooth; anterior parietal tooth 
very near columellar tooth, strong; posterior 
parietal tooth very small, about mid-length of 
aperture; outer lip thin, sharp. Protoconch 
smooth, globose; nuclear whorls deeply em- 
bedded in first whorl of teleoconch. 

Radula with 55 to 79 teeth in a row. Central 
tooth at same level as lateral teeth; base 
broad, triangular, anteriorly emarginate; 
crown small, tricuspid. Base of lateral teeth 
quadrangular, weakly bent medially; crown 
less than half length of base, with large me- 
socone, small ectocone. Transitional teeth 
with one endocone. Marginal teeth wide, 
pectinate, with as many as six ectocones. 

Animal whitish to rusty brown, translucent. 
Foot not divided transversely, posteriorly en- 
tire, round. Eyes lacking. Tentacles short, 
subcylindric. Hermaphroditic duct dilated an- 
teriorly into a pouch-like seminal vesicle; an- 







í 


^ 






../ 


r^"-^ 






r^ 










Vv 


Z.^^- ■, 








7 




Ч. 






■ \ 




o-^ 


^ 






^ 




J 






1 


Í 





FIG. 173. Creedonia succlnea, geographic distribu- 
tion. 



terior mucous gland covering posterior half of 
spermoviduct; vas deferens free from penis. 
Connectives of visceral ring very short. 

Remarks: Since its introduction by Dall (1 894) 
the genus Microtralia has been considered to 
belong to very different taxonomic groups. Its 
uncertain taxonomic position Is the result of 
the different weights given by different au- 
thors to the various taxonomic characters. 
The etymology of the word implies similarity to 
Tralla, a member of the Melampinae. Dall 
(1 894) tentatively placed Microtralia in the ge- 
nus Auricula [= Ellobium], a member of the 
Ellobiinae. Thiele (1931) considered Microtra- 
lia a subgenus of Melampus. Powell (1933), 
although recognizing the uniqueness of the 
genus, followed Qdhner's (1925) radula- 
based classification and placed his Rangito- 
toa, here considered a junior synonym of Mi- 
crotralia, in the Melampinae. Powell stressed 
the radular affinities of his genus with the 
Carychiinae. Morton (1955b), on the basis of 
anatomy and habitat preferences, placed 
Rangitotoa [= Microtralia] within the Pedipe- 
dinae. Zilch (1959) treated Microtralia as a 
subgenus of Melampus, and he considered 
Rangitotoa as a separate genus of the 
Melampinae. Abbott (1974) considered Mi- 



232 



MARTINS 



crotralia a genus of the subfamily Cassiduli- 
nae. 

Although the shell is not typical of the 
Pedipedinae, the dentition of the inner lip and 
the protoconch of Microtralla are similar to 
those of the more solid Pseudomelampus 
and Sarnia (Figs. 180, 181). The central and 
lateral teeth of the radula of this Eastern At- 
lantic genus closely resemble those of Pe- 
dipes, but the pectinate marginal teeth with 
as many as six ectocones are very similar 
to those of Pseudomelampus (Martins, per- 
sonal observation). Analysis of the reproduc- 
tive and nervous systems indicate the sys- 
tematic position of Microtralia within the 
Pedipedinae. 

The Neozealandic Rangitotoa insularis 
Powell, 1933, is quite similar to the West In- 
dian Microtralia occidentalis (Pfeiffer, 1854), 
especially in shell and radular characters, 
and Climo (1982) considered them conspe- 
cific (Fig. 179). 

Habitat: These animals live near the high- 
tide mark, under rocks partly buried in mud 
(Powell, 1933). In West Indian mangroves M- 
crotralia lives in the black sediment at the 
high-tide mark, preferably under rotting, half- 
buried branches (Martins, personal observa- 
tion). 

Range: Sporadic records from Easter Island 
(Rehder, 1980), Hawaii (Pease, 1869), New 
Zealand (Powell, 1933), Japan (Habe, 1961) 
and South Africa (Turton, 1932) indicate an 
Indo-Pacific distribution. In the West Indian 
region the genus is represented by Microtra- 
lia occidentalis (Pfeiffer). 

Microtralia occidentalis (Pfeiffer, 1 854) 
Figs. 174-178, 182-193 

Leuconia occidentalis Pfeiffer, 1854b: 155 
[Cárdenas, Cuba; location of type un- 
known]; H. & A. Adams, 1855b: 248; 
Pfeiffer, 1856a: 157; Pfeiffer, 1876: 370; 



Arango y Molina, 1880: 61; Crosse, 
1890: 260. 

Tralia (Alexia?) minúscula Dali in Simpson, 
1889: 69 [Magill's Bay, Tampa, Florida, 
and Exuma Island, Bahamas, herein re- 
stricted to Magill's Bay, Tampa, Florida; 
lectotype herein selected USNM 61211 
(Fig. 174); two paralectotypes USNM 
859503]. 

Tralia minúscula Dali. Dalí, 1889: 92. 

Auricula ? (Microtralia) minúscula (Dali). Dali, 
1894: 117, fig. 7 [Fig. 175]. 

Leucopepla occidentalis (Pfeiffer). Peile, 
1926: 88. 

Microtralia occidentalis (Pfeiffer). Pilsbry, 
1927: 125; Morrison, 1951b: 10; Abbott, 
1974: 334 [not figured; fig. 4105, errone- 
ously referred to this species, represents 
Myosotella myosotis]; Jensen & Clark, 
1986: 456 [fig. on page 456, wrongly 
stated to represent this species, is of 
Myosotella myosotis]. 

Auriculastrum (Microtralia) minusculum (Dall). 
C.W. Johnson, 1934: 159. 

Auriculastra nana Haas, 1950: 197, pi. 22, 
figs. 1 , 2 [Lover's Lake, St. George's Is- 
land, Bermuda; holotype FMNH 30169 
(not seen); paratype ANSP 212177 (Fig. 
176)]. 

Melampus (Microtralia) minusculus (Dall). 
Zilch, 1959: 65, fig. 208. 

Description: Shell (Figs. 174-178, 182-184) 
to 3.8 mm long, subcylindric, fragile, translu- 
cent, white to yellowish. Spire low to moder- 
ately high; whorls to five and three-fourths, 
weakly convex, sculptured with very fine, un- 
dulating spiral lines that extend over body 
whorl. Body whorl about 80% of shell length, 
crossed by faint, compact growth lines. Ap- 
erture about 90% of body whorl length, nar- 
row; inner lip with three teeth on anterior half; 
columellar tooth small, oblique, twisted; an- 
terior parietal tooth strong; posterior parietal 
tooth very small, sometimes reduced to a 



FIGS. 174-184. Microtralia, Rangitotoa, Pseudomelampus, Sarnia. (174) Tralia (Alexia?) minúscula Dali, 
lectotype (USNM 61211), Magill's Bay, Tampa, Florida, si 3.5 mm. (175) Auricula? (Microtralia) minúscula 
Dall, Atkins Island, Bahamas (USNM 127487), si 2.3 mm; figured by Dall (1894, fig. 7). (176) Auriculastra 
nana Haas, paratype (ANSP 212177), Lover's Lake, Bermuda, sl 3.2 mm. (177) M. occidentalis (Pfeiffer), 
Hungry Bay, Bermuda, sl 3.5 mm. (178) M. occidentalis, Hungry Bay, Bermuda, sl 3.6 mm. (179) R. insularis 
Powell, paratype (ANSP 242319), Rangitoto Island, Auckland, New Zealand, sl 3.2 mm. (180) P. exiguus 
(Lowe), lectotype (BMNH 1 875.1 2.31 .1 09), Madeira, sl 5.8 mm. (1 81 ) S. frumentum (Petit), syntype? (BMNH 
1843.11.24.58), Lima, Peru, sl 7.0 mm. (182) M. occidentalis, top view of spire and protoconch. Plantation 
Key, Florida. (183) M. occidentalis, Hungry Bay, Bermuda, sl 3.1 mm. (184) M. occidentalis, lateral view of 
spire and protoconch. Hungry Bay, Bermuda. Scale 1 mm. 



WESTERN ATLANTIC ELLOBIIDAE 



233 




FIGS. 174-184. 



234 



MARTINS 




FIGS. 185-188. Microtralia occidentalis, radular teeth. (185) Hungry Bay, Bermuda, si 3.9 mm. (186) Grassy 
Key, Florida. (187, 188) Hungry Bay, Bermuda, si 3.9 mm. Scale 20 цт. 



barely visible callus at mid-length of aperture; 
outer lip sharp, parallel to body whorl, sinu- 
ous. Inner wall of whorls occupying less than 
one-quarter of body whorl (Fig. 178). Proto- 
conch globose; nuclear whorls deeply invo- 
luted in first whorl of teleoconch; only small 
portion of lip showing (Figs. 182, 184). 

Animal whitish to rusty brown; tentacles 
short, subcylindric, with tip weakly pointed or 
somewhat flat and expanded. Eyes lacking. 
Mantle skirt whitish with brownish tinge along 
border. Palliai cavity somewhat elongate; 
kidney broadly triangular, anteriorly rounded, 
covering most of palliai cavity; pneumo- 
stomal and anal openings prolonged by a 
tube-like flap of mantle skirt; anal gill well de- 
veloped. 

Radula (Figs. 185-189) having formula [15 
+ (3 + 1 6) + 1 + (1 6 + 3) = 1 5] X 95. Crown of 
central tooth small, as wide as posterior end 
of base, tricuspid; mesocone small, blunt to 
weakly pointed; ectocones very small but 
well defined. Lateral teeth 12 to 18; crown 



1L 2L 16L 1T 2T 3T 




FIG. 189. Microtralia occidentalis, radula, Grassy 
Key, Florida. Scale 10 |.im. 

wider than base, bicuspid; mesocone 
broadly rounded anteriorly, becoming more 
pointed and longer toward marginal teeth. 
Transitional teeth two to three, with small en- 
docone, thinner and longer ectocone. Mar- 



WESTERN ATLANTIC ELLOBIIDAE 



235 





per 



FIG. 190. Microtralia occidentalis, stomach, Ber- 
muda. Scale 1 mm. 



FIG. 191. Microtralia occidentalis, reproductive 
system, Hungry Bay, Bermuda. A, B, transverse 
sections and their locations. Scale 1 mm. 



ginal teeth 13 to 19; base short and wide, 
vuith lateral flare, on v\/hich endocone of next 
tooth articulates; Crown gradually widening 
and mesocone gradually becoming shorter 
and thinner toward margin; first marginal 
tooth with two ectocones; additional ecto- 
cones appearing on fourth, eighth and twelfth 
marginal teeth; sometimes a sixth ectocone 
appears on twelfth marginal tooth in some 
rows. 

Digestive system (Fig. 190) having diges- 
tive gland with two subequal lobes. Posterior 
crop dilated, receiving anterior diverticulum 
just before joining stomach. Anterior portion 
of stomach thin, with inner thickening be- 
tween entrance of esophagus and exit of 
intestine; mid-stomach gizzard-like, thickly 
muscular; gastric caecum thin, dilated, re- 
ceiving posterior diverticulum at junction with 
gizzard. 

Reproductive system (Fig. 191) with 
ovotestis acinose, trilobed, conical, at poste- 
rior tip of visceral mass, covering stomach; 
hermaphroditic duct straight, with anterior, 
pouch-like seminal vesicle connecting with 
convoluted fertilization chamber; albumen 
gland and posterior mucous gland large; an- 
terior mucous gland and prostate gland cov- 
ering posterior half of spermoviduct; bursa 
duct as long as spermoviduct, thick, empty- 



ing near opening of vagina; bursa oval-elon- 
gate; vas deferens separates from oviduct 
near opening of vagina. Penis short, thick; 
associated vas deferens free, somewhat 
longer than penis; penial retractor about as 
long as penis, inserting on penis subapically, 
attaching to anterior portion of floor of palliai 
cavity. 

Nervous system (Fig. 192) with cerebral 
commissure somewhat shorter than width of 
cerebral ganglion; left cerebropleural and 
cerebropedal connectives longer than right 
ones; connectives of visceral ring very short, 
causing agglomeration of ganglia; pedal 
commissure short but conspicuous. Cerebral 
ganglia largest; pleural ganglia well devel- 
oped; left parietal ganglion very small; right 
parietal ganglion and visceral ganglion about 
same size. Penial nerve branching from me- 
dial lip nerve. 

Remarks: Originally Pfeiffer (1 854b) assigned 
Microtralia occidentalis to the genus Leuco- 
nia Gray, 1840, which, because it was preoc- 
cupied, was renamed Leucopepla by Peile 
(1926). Pilsbry (1927) showed that on the ba- 
sis of shell characters Microtralia occidentalis 
could not be placed in Leucopepla [= Auricu- 
linella]. The latter genus belongs in the Ello- 
biinae on the basis of its nervous and repro- 



236 



MARTINS 




«g p>g 



piprc pig 



FIG. 192. Microtralia ocddentalis, central nervous 
system, Hungry Bay, Bermuda. Scale 1 mm. 



ductive systems, and Microtralia (see re- 
marks under the genus) rightly belongs in the 
Pedipedinae. 

Dall (1889), apparently unaware of Pfeif- 
fer's name, described Tralia (Alexia?) minús- 
cula (Fig. 174) for which he created, in 1894, 
the subgenus Microtralia, tentatively remov- 
ing it to the genus Auricula. The odd combi- 
nations of names representing such different 
groups indicate the extent to which Dall was 
confused about the relationships of this small 
species. 

Microtralia occidentalis shows some mor- 
phological variation within populations and 
across its geographical range. Bermudian 
specimens are brownish and have the tips of 
the tentacles somewhat flat and broad. Flo- 
ridian specimens are usually whitish, some- 
times yellowish brown, and the tentacles are 
subcylindrical with blunt or weakly pointed 
tips. Bahamian examples are rusty brown and 
the tips of the tentacles are intermediate in 
shape between Bermudian and Floridian 
specimens. The radulae of specimens from 
Bermuda have rounder and somewhat shorter 
cusps than do those from Florida, but other- 
wise show no other morphological differ- 
ences. Intrapopulational variations in shell 
morphology, especially the height of the spire 
and the strength of the apertural teeth, occur 
throughout the range of the species. 

Haas (1950) apparently was unaware of 
Pfeiffer's or Dall's names when he introduced 
Auriculastra nana from Bermuda, for he 
did not refer to either author in the original 
description. Haas' species (Fig. 176) does 
not differ from Microtralia occidentalis and it 



must therefore be considered a junior syn- 
onym of the latter. 

Climo (1982), as noted under the remarks 
for the genus, synonymized Rangitotoa insu- 
laris Powell with Microtralia occidentalis, con- 
sidering the former to have been introduced 
in New Zealand and possibly also in Rapa Iti 
Island and Easter Island. I concur with Cli- 
me's taxonomic decision about the genera, 
on the basis of the conchological and radular 
similarities; however, the widespread distri- 
bution of the genus (see the remarks for the 
genus) and the anatomical differences ob- 
served in Microtralia alba (Gassies, 1865) 
from Hong Kong (Martins, 1992), preclude an 
immediate synonymization of both species. 

An anatomical peculiarity of Microtralia oc- 
cidentalis is the absence of eyes, confirmed 
by histological examination. Concealment of 
the eyes under the skin has been reported for 
several species of the genus Ellobium (Pelse- 
neer, 1894a: 75, note 1). In the West Indian 
species Ellobium (A.) dominicense the eyes, 
although covered by thick skin, are readily 
visible. 

The shell of Microtralia occidentalis is not 
confused easily with that of any other West 
Indian ellobiid. It can resemble the very thin- 
shelled juveniles of some populations of Tra- 
lia ovula, however. Microtralia has a large, 
rounded protoconch, faintly incised, undulat- 
ing lines on the spire and a posterior parietal 
tooth that is anterior to the mid-length of the 
aperture. In Tralia ovula the apex is mu- 
cronate, the spire has marked, pitted lines 
and the posterior parietal tooth is in the pos- 
terior half of the aperture. 

Microtralia commonly occurs with Pedipes 
ovalis, Laemodonta cubensis, Blauneria het- 
eroclita and Creedonia succinea and is 
readily distinguished from them. Pedipes is 
globose and has a rounded, strongly dentate 
aperture, Laemodonta is oval-elongate and 
hirsute and has a heavily dentate aperture, 
Blauneria has a sinistral shell and Creedonia 
has a truncated spire and very different inner 
lip dentition. 

Habitat: Microtralia occidentalis lives at or 
above the high-tide mark, buried in the 
sediment sometimes 10 to 15 cm deep, in 
the company of Blauneria heteroclita and 
Creedonia succinea. The animals are quite 
common under partly buried, rotting wood or 
porous rocks, and on the roots of mangrove 
propagules, on which Laemodonta cubensis 
and Pedipes ovalis also abound. 



WESTERN ATLANTIC ELLOBIIDAE 



237 







î; 


\ 






■7 








Г" 


4- 


». 






и 


^C 


». 






^^"^^4. 




^-4 


"v 










Q-- 


^ 






Ч 




_y 








Í 





FIG. 193. Microtralia occidentalis, geographic dis- 
tribution. 



Range: Bermuda; Clearwater, Florida, south 
to the Florida Keys and the Greater Antilles 
(Fig. 193). 

Specimens Examined: BERMUDA (USNM 
250297); Fairyland (ANSP 99075; USNM 
208069); Old Road, Shelly Bay (A.M.); Lover's 
Lake, St. George's (ANSP 212172); near St. 
George's (ANSP 1008220); Castle Harbour, 
near Harrington House (ANSP 143322); Coo- 
per's Island (ANSP 131645); Hungry Bay 
(A.M.); S End of Ely's Harbour (A.M.); Man- 
grove Bay (A.M.). FLORIDA: N of Tavernier 
Creek, Key Largo (A.M.); S of Ocean Drive, 
Plantation Key (A.M.); Lignumvitae Key 
(ANSP 156682); Long Key (A.M.); Grassy 
Key (A.M.); Crawl Key (A.M.); Bahia Honda 
Key (ANSP 104108); Big Pine Key (ANSP 
104102); W of Kohen Avenue, Big Pine Key 
(A.M.); Big Torch Key (ANSP 104001; A.M.); 
Sugarloaf Key (ANSP 89558); Boca Chica 
Key (ANSP 152503; USNM 270350); Semi- 
nole Point (ANSP 105409); Blue Hill, Hors Is- 
land (ANSP 99199); Captiva Island (ANSP 
131836); McGill's Bay, near Tampa (USNM 
61211, 859503); Boca Ciega Bay (ANSP 
9571); Pinellas Point (USNM 83255); Clear- 
water Island (ANSP 9351). BAHAMA IS- 
LANDS: GREAT ABACO ISLAND: Mores Is- 



land (MCZ 294207); ANDROS ISLAND: South 
Mastic Point (A.M.); Stafford Lake (ANSP 
294338); Mangrove Cay (USNM 270214b); 
NEW PROVIDENCE ISLAND: W of Clifton 
Point (A.M.); E of Clifton Pier (A.M.); shore 
of Millars Road (A.M.); Bonefish Pond 
(A.M.); AKLINS ISLAND: Pinnacle Point 
(USNM 390857a); SAN SALVADOR (USNM 
127487): Bob's Key, S. Ferdinand (USNM 
360499). CUBA (ANSP 22482): near Habana 
(ANSP 130794). JAMAICA: Falmouth (ANSP 
397269); Robin's Bay (USNM 441980, 
442113); Kingston (USNM 395452b); Rio Co- 
bre, Port Royal (USNM 426889); Hunt's Bay 
(USNM 441642); Rock Fort (USNM 467164). 
HAITI: Gonave Island (USNM 380184). DO- 
MINICAN REPUBLIC: Rio Guayabin by Sa- 
baneta Road (ANSP 160398). PUERTO 
RICO: Puerta de Tierra, San Juan (A.M.); Pu- 
erto Real (A.M.). 

Genus Leuconopsis Hutton, 1884 

Leuconopsis Hutton, 1884: 213. Type spe- 
cies by monotypy: Leuconopsis obsoleta 
(Hutton, 1878). 

Apodosls Pilsbry & McGinty, 1949: 9. Type 
species by monotypy: Apodosis novi- 
mundi Pilsbry & McGinty, 1949. 

Description: Shell to 4 mm long, oval-conic to 
oblong-conic, somewhat thin to solid. Spire 
low to moderately high, with as many as six 
and one-half flat, striated whorls. Body whorl 
about 80% of shell length. Aperture about 
75% length of body whorl, approximately 
oval, posteriorly angulate; inner lip with strong 
submedian columellar tooth, usually with 
weak anterior secondary tooth; outer lip 
sharp. Protoconch smooth; nuclear whorls 
embedded in first whorl of teleoconch. 

Radula with 87 to 1 1 1 teeth in a row. Base 
of central tooth widened anteriorly, sharply 
constricted posteriorly; crown thin, falciform; 
mesocone long, sharp. Base of lateral teeth 
abruptly bent medially at half length; crown as 
wide as base, with strong endocone. Transi- 
tional teeth lacking. Marginal teeth with strong 
mesocone, weaker endocone and ectocone. 

RemarlKs: The genus Apodosis was created 
by Pilsbry & McGinty (1949) for the smallest 
and rarest West Indian ellobiid. In the original 
description the authors stated (p. 10) that 
they were "strongly inclined to treat Apo- 
dosis as a subgenus of the antipodal genus 
Leuconopsis Hutton." The shape of the shell, 
oblong-conic in the Atlantic species vs oval- 



238 



MARTINS 



conic in the type species (Fig. 217) the unim- 
pressed suture and the inner thickening of 
the outer lip led them to establish a new ge- 
nus. Examination of additional specimens of 
Leuconopsis novimundi revealed that the 
thickness of the outer lip varies with the 
thickness of the shell, and that the distinct 
thickened outer lip actually does not appear 
in some thin-shelled specimens. This varia- 
tion was observed in Leuconopsis manningi 
n. sp. from Ascension Island and in Leu- 
conopsis rapanuiensis Rehder, 1980, from 
Easter Island. The other characters men- 
tioned by Pilsbry & McGinty are significant 
only at the specific level. The most obvious 
generic shell characters are the absence of a 
parietal tooth and the presence of a weak 
secondary columellar tooth just anterior to 
the primary submedian columellar tooth. This 
columellar structure is reminiscent of Pe- 
dipes, Marinula and Creedonia. 

Powell (1933) illustrated the radula of Leu- 
conopsis obsoleta (Hutton, 1878). The mor- 
phology of the teeth is very similar to that of 
the West Indian Apodosis novimundi. On the 
basis of shell and radular characters, Apo- 
dosis Pilsbry & McGinty must be considered 
a junior synonym of Leuconopsis Hutton. 

IHabitat: The genus lives intertidally under 
rocks (Hutton, 1884). Powell (1933: 150) 
found Leuconopsis obsoleta "in sheltered 
harbour bays towards high-tide, . . . and on 
cliffs, just above high-tide mark, in situations 
where fresh-water seepage occurs." I col- 
lected Leuconopsis novimundi on New Prov- 
idence Island, Bahama Islands, in crevices of 
cliffs, just above high tide, but I did not see 
any indication of freshwater seepage. 

Range: The genus Leuconopsis occurs in 
the Pacific in Australia, New Zealand and 
Easter Island. In the Atlantic it is represented 
by Leuconopsis novimundi (Pilsbry & Mc- 
Ginty) from the Florida Keys, Bahamas and 
Jamaica, and by Leuconopsis manningi, 
herein described, known only from Ascen- 
sion Island. A possible third species from St. 
Thomas is left unnamed owing to lack of suit- 
able material. 

Leuconopsis novimundi 

(Pilsbry & McGinty, 1949) 

Figs. 194-204 

Apodosis novimundi Pilsbry & McGinty, 
1949: 10, pi. 1, fig. 1 [Clifton Bluff, New 
Providence, Bahamas; holotype ANSP 



185474a (Fig. 194)]; Morhson, 1951b: 9; 
Zilch, 1959: 70, fig. 227; Franc, 1968: 
525; Abbott, 1974: 334, fig. 4102. Non 
"Pilsbry & McGinty" Rosewater, 1975 
[misindentification of Leuconopsis man- 
ningi Martins n. sp.]. 

Description: Shell (Figs. 194-197) to 3.4 mm 
long, oblong-conic, solid, uniformly light 
yellow to pale brown. Umbilical area marked 
by shallow excavation. Spire moderately 
high, whorls as many as six and one-half, 
flat and heavily sculptured with numerous 
spiral cords, intersected by compact axial, 
somewhat regularly spaced, fine growth 
lines, giving shell a matte appearance. Body 
whorl convex, about 75% of shell length and 
with same sculpture as spire. Aperture about 
70% body whorl length, subaxial, narrowly 
ovate; inner lip with partly hidden tooth at 
point of juncture of columella and parietal 
wall; occasionally secondary columellar 
tooth present as faint callosity just anterior to 
columellar tooth; outer lip sharp. Protoconch 
oblong, smooth, transparent, with sinuous lip 
(Fig. 197). 

Animal whitish gray; foot dirty white, trans- 
versely divided; tentacles short, transparent, 
subcylindric, with rounded tip; mantle skirt 
slightly lighter than rest of animal. 

Radula (Figs. 198-201) having formula 
(33 + 1 + 1 + 1 + 33) X 75+. Base of central 
tooth with quadrangular anterior half, round 
at tip; width of posterior half abruptly re- 
duced to half; crown as wide as posterior half 
of base, falciform; mesocone just over half 
length of base, pointed. Lateral teeth bicus- 
pid; mesocone sharp, as long as, but stron- 
ger than, that of central tooth; endocone 
sharp, almost as long and strong as meso- 
cone. Marginal teeth tricuspid; ectocone be- 
coming as long as endocone; mesocone be- 
coming smaller, but remaining the strongest 
cusp. 

Digestive system with posterior crop wide, 
with strong internal folds; stomach very mus- 
cular, with gastric caecum where posterior 
diverticulum empties. 

Reproductive system (Fig. 202) semidiau- 
lic, with vas deferens separating from oviduct 
almost at half-length of palliai gonoduct; an- 
terior mucous gland covers spermoviduct 
nearly to separation of vas deferens; bursa 
duct empties near female opening. Penial 
complex dilated, pouch-like in mid-section; 
posterior section thinner, coming out of 
pouch as blunt diverticulum; penial retractor 



WESTERN ATLANTIC ELLOBIIDAE 



239 




FIGS. 194-200. Leuconopsis novimundi (Pilsbry & McGinty), Clifton Bluff, New Providence, Bahamas. (194) 
Holotype (ANSP 185474a), sl 3.36 mm. (195) Shell length 2.73 mm. (196) Lateral view of spire and proto- 
conch. (197) Top view of spire and protoconch. (198) Central, lateral and marginal teeth of radula. (199) 
Marginal teeth of radula. (200) Marginal teeth of radula. Scale, Figs. 196, 197, 1 mm; Figs. 198-200, 20 |jm. 



multifid, short, attaching to end of posterior 
section of penis subapically; vas deferens 
free, entering penis at base of thinner poste- 
rior section. 

Nervous system (Fig. 203) with cerebral 
ganglia largest; left pleural ganglion larger 
than right one; left parietal ganglion much 
smaller than right one; visceral ganglion 



с IL 2L 10L 1М 7М 26М 27М 31М 




FIG. 201. Leuconopsis novimundi, radula, Clifton 
Bluff, New Providence, Bahamas. Scale 10 |.im. 



MARTINS 




FIG. 202. Leuconopsis novimundi, reproductive system, Clifton Bluff, New Providence, Bahamas. Penis 
drawn under camera lucida, palliai gonoducts reconstructed from histological sections. A-L, transverse 
sections and their locations. Scale 1 mm. 



about as large as right parietal ganglion. Ce- 
rebral commissure somewhat longer than 
width of cerebral ganglion; right and left cere- 
bropedal and cerebropleural connectives 
roughly equal; left pleuroparietal connective 
very small; all other visceral ring connectives 
equal, about half length of cerebropleural 
connectives. 



Remarks: Leuconopsis novimundi shows 
some anatomical deviations from typical 
members of the Pedipedinae such as Pe- 
dipes and Creedonia (see the remarks under 
the subfamily). The origin of the vas deferens 
from the mid-section of the spermoviduct- 
vaginal tract was unexpected in this species 
because Morton (1955b) stated that the sep- 
aration of the vas deferens from the sper- 
moviduct in Leuconopsis obsoleta occurs 
at the vaginal opening, as in Ovatella [sensu 
Myosotella]. Nevertheless, Leuconopsis novi- 
mundi is placed in the Pedipedinae on the 
basis of the presence of the double columel- 
lar tooth in the aperture, the shape of the 
crown of the central and lateral teeth, the 
prostate and anterior mucous gland not 




FIG. 203. Leuconopsis novimundi, central nervous 
system, Clifton Bluff, New Providence, Bahamas. 
Scale 1 mm. 

reaching the female opening, and the rela- 
tively short visceral nerve ring, as compared 
to that of the Pythiinae or Ellobiinae. 



WESTERN ATLANTIC ELLOBIIDAE 



241 



Rosewater (1975) erroneously identified a 
small Leuconopsis from Ascension Island 
as Apodosis novlmundi. These specimens 
(USNM 735149, 859015) differ from Leu- 
conopsis novimundi in the differently sculp- 
tured shell that lacks the matte appearance 
and in the readily visible secondary columel- 
lar tooth. They represent a previously unde- 
scribed species that is introduced as Leu- 
conopsis manningi n. sp. in this report (Figs. 
205, 206). The protoconch of Leuconopsis 
novimundi is very similar to that of Leuconop- 
sis manningi in having a sinuous lip (Figs. 
207, 208), a characteristic lacking in Leu- 
conopsis rapanuiensis (Fig. 216). 

Leuconopsis novimundi is readily distin- 
guished from all other Western Atlantic ello- 
biids by its oval-elongate shell that has a 
matte appearance and by its lack of parietal 
teeth in the aperture. 

Habitat: The two specimens collected by R. 
Robertson in 1964 on Pigeon Cay, Bimini, in 
algae on mangrove roots were probably the 
first ones to be collected alive. All other spec- 
imens in museum collections, including those 
of Pilsbry and McGinty, seem to have been 
obtained from beach drift. Despite thorough 
field work and patient rock-combing, all but 
one of the specimens I found alive came from 
a cave at the western tip of Clifton Bluff (Clif- 
ton Pt.), New Providence Island, Bahamas, 
kindly indicated to me by T. L. McGinty. The 
cave formed from a double crack in the coral 
bed, running from sea to shore. It is open 
above, so direct sunlight illuminates it a few 
hours a day. At high tide water enters the 
main opening from the ocean, as well as the 
bottom of the double crack. One specimen 
was found among stones that had collected 
in one such crack, just above high-tide mark. 
Eight others were found in the crevices as 
deep as 20 cm in the wall and were obtained 
by chipping away the wet layers of coral in a 
band about 15 cm wide just above the black 
zone. The animals apparently feed on the de- 
tritus that collects in these crevices. The 
eight specimens were found within a radius 
of about 20 cm, together with Pedipes ovalis, 
Laemodonta cubensis and young Melampus 
(D.) monile. The other live specimen was 
found at Morgan's Bluff, Andres Island, Ba- 
hamas, under stones at the high-tide mark of 
a tidal pool. 




Range: Florida 
(Fig. 204). 



Keys, Bahamas, Jamaica 



FIG. 204. Leuconopsis novimundi, geographic dis- 
tribution. 



Specimens Examined: FLORIDA: Indian 
Key (USNM 492557a). BAHAMA ISLANDS: 
GRAND BAHAMA ISLAND: Gold Creek 
(ANSP 369338); Hepburn Town, Eight Mile 
Rock (ANSP 370409); Caravel Beach [John 
Jack Point], Freeport (ANSP 370225); BIMINI 
ISLANDS: N end of Pigeon Cay (ANSP 
329623); ANDROS ISU\ND: Morgan's Bluff 
(A.M.); Mangrove Cay (USNM 180462b); First 
island off Mintie Bar, SE of South Bight 
(USNM 271888); NEW PROVIDENCE IS- 
LAND: Clifton Bluff (ANSP 1 85474; A.M.). JA- 
MAICA: Jack's Bay (USNM 441915). 

Leuconopsis manningi n. sp. 

Figs. 120, 205-212 

Apodosis novimundi Pilsbry & McGinty. 
[Type locality: English Bay, Ascension Is- 
land; holotype USNM 859015 (Fig. 205); 
11 paratypes USNM 859015 (Fig. 
206)]. Rosewater, 1975: 23. Non Pilsbry 
& McGinty, 1949. 

Description: Shell (Figs. 205-208) to 2.1 mm 
long, ovate, solid, uniformly pale to dark 
brown, smooth, shiny. Umbilical excavation 
very weak. Spire short, whorls as many as 
five and one-fourth, flat, sculptured with two 



242 



MARTINS 







JWP^'^^^lli^lj^^ 









FIGS. 205-211. Leuconopsls manningi n. sp., English Bay, Ascension Island. (205) Holotype (USNM 
859015), sl 2.02 mm. (206) Paratype (USNM 859015), sl 1.58 mm. (207) Lateral view of spire and proto- 
conch. (208) Top view of spire and protoconch. (209) Central and lateral teeth of radula. (210) Marginal teeth 
of radula. (211) Marginal teeth of radula. Scale, Figs. 207, 208, 1 mm; Figs. 209-211, 20 |.im. 



to seven incised spiral lines on shoulder in 
adults, juveniles often spirally striated on en- 
tire length; growth lines very faint. Aperture 
75% of body whorl length, ovate; inner lip 
with strong posterior columellar tooth about 
mid-length of aperture, with conspicuous but 
much smaller anterior secondary tooth; outer 
lip sharp. Protoconch oblong, smooth, trans- 
parent, dark brown, with sinuous lip. 



Radula (Figs. 209-212) having formula 

(32 + 11 + 1 + 11 + 32) X 70+. Radular morphol- 
ogy as in Leuconopsis novimundi. 
Animal unknown. 

Remarks: Leuconopsis manningi was first 
mentioned in the literature by Rosewater 
(1975), who misidentified it as Apodosis 
novimundi. This new species differs from 



WESTERN ATLANTIC ELLOBIIDAE 



243 



с IL 2L 11L IM 




FIG. 212. Leuconopsis manningi, radula, Ascen- 
sion Island. Scale 10 ¡.im. 

Leuconopsis novimundi in the ovate shape 
of the shell, the proportionately longer, 
nonmatte body whorl that usually has two 
incised lines on the shoulder, the larger ap- 
erture and the conspicuous secondary col- 
umellar tooth. Leuconopsis manningi is 
closely related to Leuconopsis rapanuiensis 
Rehder, 1980, from Easter Island (Figs. 214- 
216). The secondary columellar fold of the 
latter is farther foreward than in Leuconopsis 
manningi, the protoconch is stouter and has 
a rounded instead of sinuous lip. 

The single radula studied was obtained by 
breaking the shell of a dried aninnal; the apex 
of the shell was used for the SEM study of the 
protoconch. 

Following the suggestion of the late J. 
Rosewater I name this species for R. B. Man- 
ning, who collected the specimens in 1971. 

Habitat: Intertidal pools, subtidal rocky 
shore, with some coarse sand (from USNM 
label). 

Range: English Bay, Ascension Island (Fig. 
120). 

Leuconopsis sp. 
Fig. 213 

Description: Shell (Fig. 213) 4 mm long, oval- 
conic, solid, white. Spire moderately high, 
with about six weakly convex whorls. Body 
whorl 77% of shell length. Aperture semilu- 
nate, 67% of body whorl; inner lip with mod- 
erately strong, horizontal columellar tooth 
just anterior to mid-length of aperture; obvi- 
ous secondary tooth somewhat anterior to 
previous one; outer lip sharp. 

Remarl<s: A single specimen from St. Thom- 
as, Virgin Islands, originally from the Swift 
collection (now ANSP 22599), differs from the 
other Atlantic species of Leuconopsis in its 
wider body whorl, in its anteriorly less ex- 
panded outer lip, which gives the aperture a 
semilunate aspect, and in its conspicuous 
secondary columellar tooth at some distance 
anterior to the primary tooth. The example is 



undoubtedly a beach specimen, a fact that 
might account for the absence of any visible 
sculpture. 

I am reluctant to erect a new species upon 
a single worn specimen; the naming of this 
probably new species must await collection 
of more material. 

Subfamily Melampinae Pfeiffer, 1853 

Melampinae Pfeiffer, 1 853a: 8 [corrected from 
Melampea by H. & A. Adams, 1855b]. 

Melampodinae Fischer & Crosse, 1880: 5 
[unjustified emendation]. 

Description: Shell to 23 mm long. Spire low 
to high. Body whorl usually more than 75% of 
shell length. Aperture elongate, narrow; one 
columellar tooth; one to five parietal teeth; 
outer lip internally smooth or with as many as 
18 riblets. Protoconch nipple-like, smooth, 
with spiral axis perpendicular to columellar 
axis of teleoconch; nuclear whorls only partly 
covered by first whorl of teleoconch. 

Animal white to black, generally brown; 
foot transversely divided, bifid posteriorly. 

Radula with central tooth posterior to lat- 
eral teeth, triangular, with base deeply in- 
dented; crown with narrow, sharp mesocone, 
ectocones very small or absent. Base of lat- 
eral teeth rectangular, medially bent in shape 
of boomerang, with medial node on inner sur- 
face; crown with strong mesocone pointing 
laterally, sometimes with endocone or ecto- 
cone. Transitional teeth with shorter base, 
crown more elongate posteriorly and extra 
denticle on ectocone. Marginal teeth with 
very strong mesocone, one or two denticles 
on endocone and one to eight denticles on 
ectocone; base and crown gradually become 
shorter from innermost to outermost teeth 
and denticles of ectocone gradually advance 
to same level, becoming subequal in size. 

Digestive system having mandible tripar- 
tite, of numerous longitudinal fibers; stronger 
central portion lining upper lip and folded, ta- 
pering extremities lining lateral lips. Salivary 
glands yellowish to white, long, fusiform. 
Esophagus with internal, longitudinal folds, 
ending posteriorly in a wide crop that receives 
anterior diverticulum of digestive gland; a thin 
muscular strand secures posterior crop to 
posterior portion of muscular band of stom- 
ach. Digestive gland brown to dark orange, 
bilobed; anterior lobe very large, composed of 
several lobules that empty into wide anterior 
diverticulum; posterior lobe small, located 



244 



MARTINS 




FIGS. 213-217. Leuconopsis. (213) Leuconopsis sp., St. Thomas, Virgin Islands (ANSP 22599), formerly in 
Swift collection, si 4.04 mm. (214) L. rapanuiensis (Rehder), holotype (USNM 756790), Easter Island, sl 2.87 
mm. (215) L. rapanuiensis, paratype (USNM 756238) Easter Island, sl 2.34 mm. (216) L. rapanuiensis, top 
view of spire and protoconch. (217) L. obsoleta (Hutton), Takapuna, Auckland, New Zealand (USNM 
681309), sl 2.50 mm. Scale 1 mm. 



partly beneath ovotestis, covering posterior 
left portion of stomach and emptying into 
small posterior diverticulum. Stomach glob- 
ular, tripartite; anterior portion thin, weakly 
muscular at cardiac aperture; middle portion 
surrounded by thick band of muscle around 
pyloric region; posterior portion of caecum 
thin, receiving posterior diverticulum at ante- 
rior border, just posterior to muscular band 
and near attachment of muscular strand; 



stomach attached to mantle by muscular fi- 
bers extending from region opposite opening 
of posterior diverticulum. Intestine dilates as 
it leaves the stomach anteriorly just right of 
esophagus, and has several convolutions 
in midst of digestive gland; rectum parallels 
right edge of palliai cavity; anal opening lateral 
to pneumostome, on mantle lappet. Anal gill 
bilobed, flanking rectum just posterior to 
anus. 



WESTERN ATLANTIC ELLOBIIDAE 



245 




FIGS. 218-229. Melampus (M.) coffeus (Linnaeus). (218) Lectotype (LSL), sl 18.8 mm. (219) Paralectotype 
(LSL), sl 11.0 mm. (220) Auricula biplicata Deshayes, holotype (MNHNP), sl 20.0 mm. (221) M. coffea var. 
microspira Pilsbry, holotype (ANSP 61471), Progreso, Yucatán, Mexico, sl 12.8 mm. (222) Bermuda (USNM 
1 1 421 ), sl 1 5.2 mm. (223) Grand Bahama Island, Bahamas (MCZ 1 1 6679), sl 1 7.3 mm. (224) Anegada, Virgin 
Islands (MCZ 229004), sl 18.3 mm. (225) Isla Matica, Dominican Republic (R.B.), sl 10.4 mm. (226) Juvenile, 
Puerto Real, Puerto Rico, sl 3.6 mm. (227) Tucacas, Venezuela, sl 10.5 mm. (228) Bahía [San Salvador] 
Brazil (AMNH 22434), sl 12.0 mm. (229) Boa Viagem, Brazil (MCZ 219130), sl 19.5 mm. 



246 



MARTINS 



Reproductive system of advanced semi- 
diaulic type, the short spermoviduct separat- 
ing into long, thin vagina and vas deferens 
shortly after passing posterior mucous gland; 
posterior mucous gland large, spiral, cover- 
ing only small portion of spermoviduct; pros- 
tate gland beneath posterior mucous gland, 
not discrete; anterior mucous gland absent; 
vagina running posteriorly, turning abruptly 
and following columellar muscle anteriorly; 
elbow of vagina attached by muscle fibers to 
left corner of insertion of columellar muscle. 
Bursa with short peduncle, at or very near 
proximal end of vagina. Penis long, usually 
simple; anterior vas deferens long, thin, en- 
tering penis apically; penis and posterior vas 
deferens run beneath upper tentacle retrac- 
tors, over cerebral commissure and under 
right tentacular nerve. 

Nervous system having cerebral commis- 
sure short; cerebropleural connectives about 
same length as cerebropedal connectives; 
pleuroparietal and parietovisceral connec- 
tives very short. 

Remarks: Baker (1963) showed that, al- 
though the word Melampus has its origin in 
the Greek, meaning "black foot," it was La- 
tinized and used by the Romans in the gen- 
itive case, "melampi." Hence Melampinae 
must be used instead of Melampodinae. 

During growth the radula changes consid- 
erably in shape and number of teeth (Table 4, 
Appendix). In very young animals the inner 
edge of the arms of the base of the tricuspid 
central tooth bears conspicuous promi- 
nences. The first lateral tooth can be either 
tricuspid or bicuspid. The marginal teeth 
have an ectocone that becomes serrate, car- 
rying as many as eight subequal cusps. As 
the animal grows, certain characteristics are 
retained, such as the splitting of the en- 
docone and ectocone. Others are enhanced, 
such as the serrations on the lateral edge of 
the crown of the marginal teeth of young 
Melampus s. s. before the ectocone be- 
comes a distinct cusp. Some characteristics, 
such as the ectocone and endocone of the 
lateral teeth, become lost in most species. 
Even in adults the same tooth in adjacent 
rows might be inconsistent. The characteris- 
tics given in the description must be consid- 
ered as the general pattern in adult individu- 
als. 

In all animals examined the stomach 
agrees with Koslowsky's (1933) and Marcus 
& Marcus' (1965a) descriptions, rather than 



with Morton's (1955c) account, which did not 
record the presence of the caecum and pos- 
terior diverticulum. No evidence was found to 
support Marcus & Marcus' statement that the 
stomach of Melampus gundlachi Pfeiffer, 
1 853 [= Melampus (M.) bidentatus Say, 1 822] 
is radically different from that of other West 
Indian Melampinae. 

Only two genera compose the subfamily 
Melampinae: Melampus Montfort and Tralla 
Gray. Melampus is easily distinguished from 
Tralla on the basis of its shell. Melampus has 
a much narrower aperture than does Tralla, 
the dentition of the inner lip is restricted to 
the anterior half, the anterior parietal tooth, 
when present, is very small and the outer lip 
is usually interiorly ribbed. Tralla has a strong 
anterior parietal tooth and always has an- 
other conspicuous parietal tooth on the pos- 
terior half of the aperture. The outer lip is sin- 
uous and has only one ridge-like riblet 
opposite the posterior parietal tooth. Zilch 
(1959) listed Rangltotoa Powell in this sub- 
family, but results of this study led me to con- 
clude with Climo (1982) that Rangltotoa is a 
junior synonym of MIcrotralla Dall, which 
Zilch had listed as a subgenus of Melampus. 
The genus MIcrotralla belongs to the Pedipe- 
dinae by reason of the morphology of the re- 
productive and nervous systems. 

The Melampinae are separated from the 
other ellobiid subfamilies on the basis of rad- 
ula, reproductive system and nervous sys- 
tem. The serration of the ectocones of the 
marginal teeth of the radula has some parallel 
only in MIcrotralla. The nonglandular palliai 
gonoducts, the proximal position of the bursa 
duct and the long, generally thin penis are 
unique. The concentration of ganglia has 
some parallel in the Pedipedinae, but in the 
Melampinae the cerebral commissure is rel- 
atively shorter and the cerebropleural and the 
cerebropedal connectives are much longer. 

A planktonic veliger has been reported for 
several Melampinae (Morrison, 1959; Rus- 
sell-Hunter et al., 1972; Berry, 1977). This 
condition is considered primitive, retained 
from the estuarine habit of the ancestors of 
the ellobiids. 

Habitat: The Melampinae are the most com- 
mon ellobiids in the Western Atlantic, living 
mostly in salt marshes and in mangroves. 
They can occur in zones of very low salinity 
such as along the banks of rivers some miles 
inland [Melampus (M.) bidentatus, Melampus 
(D.) florldanus], or under rocks exposed to 



WESTERN ATLANTIC ELLOBIIDAE 



247 



high-tide surf [Melampus (D.) monile, Tralia 
(T.) ovula]. They are among the соглтоп gas- 
tropods found in Stephenson & Stephen- 
son's (1950) upper intertidal gray zone. 

Range: Worldwide distribution, except in the 
Mediterranean region. In the Western Atlantic 
the Melampinae extend from Newfoundland 
to southern Brazil. Species are especially nu- 
merous in the West Indian region. 

Genus Melampus Montfort, 1810 

Melampus Montfort, 1810: 319. Type species 
by monotypy: Melampus coniformis 
(Bruguière, 1789) [= Melampus coffeus 
(Linnaeus, 1758)]. Non Gray, 1865 
[Mammalia]. 

Conovulus Lamarck, 1816, pi. 459, fig. 2 a. 
b., Liste, p. 12. Type species herein des- 
ignated, Conovulus coniformis (Bru- 
guière, 1789) [= Melampus coffeus (Lin- 
naeus, 1758)]. 

Melampa "Draparnaud" Montfort. Schweig- 
ger, 1820: 739 [unjustified emendation of 
Melampus]. 

Conovula Lamarck. Schweigger, 1820: 739 
[in synonymy; unjustified emendation of 
Conovulus]. 

Conovulae Lamarck. Férussac, 1821: 104 
[unjustified emendation of Conovulus]. 

Conovolus Lamarck. Sowerby, 1839b: 10 [er- 
ror for Conovulus]. 

Conovulum Lamarck. Sowerby, 1842: 119 
[unjustified emendation of Conovulus]. 

Maelampus Montfort. Reeve, 1877, pi. 1 [in 
synonymy; error for Melampus]. 

Description: Shell ovoid, white to dark 
brown, uniform or with light spiral bands or 
axial stripes. Aperture high, narrow, with wid- 
est point above columellar tooth; first parietal 
tooth reduced or absent; outer lip sharp, with 
lirae. 

Animal grayish blue to black; tentacles 
subcylindric, pointed. 

First lateral tooth of radula with or without 
ectocone, always lacking endocone. 

Salivary glands attaching to ventral portion 
of esophagus, right one in front of left one. 
Esophagus heavily pigmented. 

Reproductive system having ovotestis of 
dark yellow radiating tubules with or without 
dark brown spots, shallow-conic to leaf-like, 
rounded or lobed at base, deeply split on 
right side; gonadial artery entering ovotestis 
from left, bifurcates and radiates, covering 
lower surface of gland. Hermaphroditic duct 



brown, moderately long, forming very convo- 
luted seminal vesicle, passing beneath pos- 
terior diverticulum. Albumen gland spiral. 
Posterior end of short, nonglandular sper- 
moviduct with pouch-like prevaginal cae- 
cum; bursa large, banana-shaped, located 
partly against mucous gland, partly embed- 
ded in digestive gland, beneath heart. Penis 
simple, thin; penial retractor usually running 
beneath albumen gland, entering between 
two major bundles of columellar muscle and 
inserting together with muscle attachment; 
often penial retractor attaches to floor of 
lung, bifurcates or runs on top of columellar 
muscle. 
Free-swimming veliger larva present. 

Remarks: Ignorance of the specific habitat of 
the supralittoral pulmonate genus Melampus 
Montfort led to taxonomic misplacement of 
the group. Some early workers tried to incor- 
porate habitat information in their classifica- 
tion schemes and therefore early 19th cen- 
tury nomenclatorial history of this genus is 
related not only to shell characters but also to 
knowledge of the habitats of species. 

Montfort (1810) separated Melampus con- 
iformis (Bruguière) [= Melampus coffeus (Lin- 
naeus)] from Bulimus Bruguière on the basis 
of apertural details, and from Auricula La- 
marck [= Ellobium Röding] and Scarabus 
Montfort [= Pythia Röding] on the basis of its 
conical shape. Bulimus Bruguière was a 
large, heterogeneous assemblage of mostly 
terrestrial and fluviatile mollusks. Montfort 
(1810: 320) seems to have had reliable infor- 
mation about the marine habitat of Melampus 
(M.) coffeus, for he specified (1810: 20), "Ce 
mollusque est marin, il vit sur les côtes de 
Cayenne, et principalement contre le rocher 
du Conètable, qui est en avant de la rade." It 
is also probable that Montfort had access to 
live or preserved material, although in the 
description he did not mention the external 
appearance of the animal. Only such an ob- 
servation would justify the choice of the ap- 
propriate name Melampus, meaning black 
foot, a conspicuous characteristic of the type 
species. 

Lamarck, apparently unaware of Mont- 
fort's work, also used shell shape and habitat 
in his classification. In 1812 he used the ver- 
nacular Conovule, Latinized by him in 1816 to 
Conovulus, for those fluviatile shells with the 
outer lip simple and sharp, which he previ- 
ously had included under Лил/'си/а. Upon be- 
ing informed that the animals in question 



248 



MARTINS 



were terrestrial, however, Lamarck (1822: 
136) suppressed Conovulus, reuniting those 
species with Auricula. Nevertheless, the name 
Conovulus continued to be used occasionally, 
either emended or as originally spelled (Beck, 
1837; Anton, 1839; Gray, 1840; Clark, 1850, 
1855). 

Lowe (1832) was convinced that the genus 
Melampus Montfort should be included 
within the marine pectinibranchs, and he 
stated, wrongly, that his Melampus aequalis 
[= Ovatella aequalis] had branchial respira- 
tion. Lowe knew of Montfort's comments on 
the marine habitat of the type species, 
Melampus (M.) coffeus, but he listed the latter 
species, without justification, among Species 
incertae: hue forsan referendae [Uncertain 
species; perhaps to be referred to this place]. 
It was this misidentification that led Gray 
(1 847a) to consider Lowe's use of Melampus 
Montfort distinct and thus erroneously to 
designate a type species. 

The genus Melampus is the predominant 
West Indian ellobiid group because of the 
number of species and abundance of individ- 
uals. Of the 18 recognized ellobiid species 
belonging to ten genera, seven are in Melam- 
pus. The very numerous individuals in salt 
marshes (Morrison, 1951a; Martins, personal 
observation) and in mangroves (Martins, per- 
sonal observation) makes them very conspic- 
uous occupants of those habitats. 

Only two subgenera are recorded for the 
Western Atlantic, Melampus s. s. and Detra- 
cia Gray, which can be separated on the ba- 
sis of apertura! morphology. In Melampus s. 
s. the columellar tooth is small and the upper 
parietal tooth is the largest of the teeth on the 
inner lip. In Detracia the columellar tooth is 
largest, usually strongly twisted, and the up- 
per parietal tooth is small and hidden. Ana- 
tomical differences reside mainly in the com- 
paratively longer separation of the foot from 
the visceral mass in Detracia, with conse- 
quent elongation of the palliai and anterior 
reproductive ducts. In Detracia the mantle or- 
gan is conspicuously pouch-like, rather than 
rounded and conforming to the general 
shape of the mantle cavity. 

The anatomical differences are related to 
the degree of resorption of the inner whorls of 
the shell. In Melampus s. s. resorption is so 
extensive that less than half of the partition of 
the body whorl remains (Figs. 225, 267), 
whereas in Detracia at least 75% of that par- 
tition remains (Figs. 302, 316, 340, 361). In 
Detracia the parietal teeth appear on the in- 



ner whorl as two conspicuous lamellae and 
the region near the columellar tooth forms a 
cavity that is occupied by the pouch-like 
mantle organ. 

Habitat: Ubiquitous in those habitats men- 
tioned for the Melampinae. 

Range: Worldwide. Most of the Western At- 
lantic species live in the West Indies, but the 
genus extends from Newfoundland to south- 
ern Brazil. 

Subgenus Melampus s.s. 

Description: Shell oval-conic, spire low, eight 
to 12 whorls; posterior parietal tooth stronger 
than columellar tooth. Animal brownish to uni- 
form black or with white markings. Medial 
edge of arms of base of central tooth of radula 
smooth or with very faint medial nodes. Vis- 
ceral mass separated from foot by half a 
whorl; mantle organ round, not pouch-like. 

Remarks: Beck (1837) used Melampus В 
[Beck {sic)] as a subgenus of Melampus Mont- 
fort. In listing the species, however, he did not 
include Melampus (M.) coffeus, the type of the 
nominate genus, which he had listed under 
the subgenus Conovulus В [Beck (sic)]. Gray 
(1847a) considered Beck's Melampus a valid 
taxonomic name and he erroneously desig- 
nated Melampus lineatus Say [= Melampus 
(M.) bidentatus Say] as type species. 

Melampus s. s. is represented in the West- 
ern Atlantic by only two species; Melampus 
(M.) coffeus (Linnaeus) and Melampus (M.) bi- 
dentatus Say. In Florida, Bermuda and the 
Greater Antilles, in which they overlap, the 
two species show a wide range of variation in 
shape and color, sometimes making their 
separation difficult. Melampus (M.) bidenta- 
tus can be recognized by the presence of at 
least one, usually two or three marked spiral 
grooves on the whorls of the spire and on the 
shoulder of the body whorl. In Melampus (M.) 
coffeus these grooves occur only on the first 
four whorls (Figs. 230, 232, 233). In addition, 
Melampus (M.) coffeus is conical, whereas 
Melampus (M.) bidentatus is more ovoid. Al- 
though variable in color, Melampus (M.) cof- 
feus characteristically has as many as five 
dark, olive-green bands on the body whorl 
and usually it has a pinkish to purple patch 
covering the columellar fold and the tip of the 
columella. In Melampus (M.) bidentatus the 



WESTERN ATLANTIC ELLOBIIDAE 



249 



bands are usually brownish and the col- 
umella is white. Anatomical differences oc- 
cur, as in the nervous system, in which the 
right parietovisceral connective is shorter 
than that in Melampus (M.) coffeus; also in 
this species the vagina is twice the length of 
the posterior vas deferens, whereas in 
Melampus (M.) bidentatus, although variable, 
both ducts are much more alike in length. 

Habitat: Melampus (M.) bidentatus is a com- 
mon inhabitant of the North American salt 
marshes and of the mangroves of the Florida 
Keys, Bermuda and the Bahama Islands. 
Melampus (M.) coffeus lives in mangroves 
from Florida to Brazil. This species has not 
been reported from salt marshes and it over- 
laps with the former species only in man- 
groves. 

Range: The subgenus Melampus has a 
worldwide distribution, not being restricted, 
as are most ellobiid groups, to the tropics. In 
the Western Atlantic the subgenus extends 
from Newfoundland, Canada, to Brazil. 

Melampus (Melampus) coffeus 

(Linnaeus, 1758) 

Figs. 218-256 

Bulla coffea Linnaeus, 1758: 729 [type local- 
ity unknown, herein designated to be 
Barbados, West Indies; lectotype herein 
selected, Linnaean collection, LSL (Fig. 
218)]. 

Voluta coffea (Linnaeus). Linnaeus, 1767: 
1 1 87; Gmelin, 1 791 : 3438; Dillwyn, 1 81 7: 
505. 

Bullmus coniformis Bruguière, 1789: 339 
[American coast, herein restricted to 
Barbados, West Indies; location of type 
unknown]. 

Melampus coniformis (Bruguière). Montfort, 
1810: 319; Lowe, 1832: 292; С В. Ad- 
ams: 1849: 42; С. В. Adams, 1851: 186; 
Shuttleworth, 1858: 73; Franc, 1968: 
525. 

Conovulus coniformis (Bruguière). Lamarck, 
1816, pi. 459, figs. 2, a. b.. Liste p. 12. 

Auricula coniformis (Bruguière). Férussac, 
1821: 105; Lamarck, 1822: 141; Menke, 
1830: 36; Gould, 1833: 67; Potiez & 
Michaud, 1838: 202; Jay, 1839: 59; 
Sowerby, 1839b: 10, fig. 298: Sowerby, 
1 842: 77, fig. 298; Küster, 1 844: 31 , pi. 4, 
figs. 14-17; Reeve, 1877, pi. 7, fig. 57. 

Pedipes coniformis (Bruguière). Blainville, 



1824: 245; Blainville, 1825: 325 [425], pi. 
37 bis, fig. 4 [erroneously listed in plate 
caption as Tornatelle coniforme]. 

Auricula biplicata Deshayes, 1830: 91 [type 
locality unknown, herein designated to 
be Barbados, West Indies; holotype 
MNHNP (Fig. 220)]; Pfeiffer, 1854b: 148. 

Melampus (Conovulus) biplicatus (Deshayes). 
Beck, 1837: 106. 

Melampus (Conovulus) coffeus (Linnaeus). 
Beck, 1837: 106. 

Auricula (Conovulus) coniformis (Bruguière). 
Anton, 1839: 48. 

Auricula conoidalis (Bruguière). Sowerby, 
1839b: 63, fig. 298; Sowerby, 1842: 187, 
fig. 298 [referred to in text as coniformis]. 

Conovulus coffee (Linnaeus). Gray, 1840: 20 
[error for coffea]. 

Auricula coniformis Férussac. Orbigny, 1841 : 
187, pi. 12, figs. 4-7 [plate caption incor- 
rect; should be 4-7, not 1-3]. 

Auricula coniformis Lamarck. Reeve, 1842: 
106, pi. 187, fig. 7. 

Auricula olivula "Moricand" Küster, 1844: 33, 
pi. 3, figs. 11-33 [Bahía, Brazil; location 
of type unknown]. 

Melampus coffea (Linnaeus). Mörch, 1852: 
38; Pfeiffer, 1854b: 147; Pfeiffer, 1856a: 
28; Binney, 1860: 4; Binney, 1865: 13, 
fig. 15; Tryon, 1866: 8, pi. 18, figs. 7, 8; 
Pfeiffer, 1876: 306; Mörch, 1878: 5; 
Fischer & Crosse, 1880: 23, pi. 34, figs. 
10, 10a; Crosse, 1890: 258; Hinkley, 
1 907: 71 ; Bequaert & Clench, 1 933: 538. 

Melampus coniformis (Lamarck). Shuttle- 
worth, 1854b: 101. 

Melampus coffeus (Linnaeus). H. & A. Adams 
1854: 9; H. & A. Adams, 1855b: 243, pi 
82, figs. 7, 7a; Binney, 1859: 162, pi. 75 
figs. 21 , 25; Poey, 1 866: 394; Nevill, 1 879 
219; Arango y Molina, 1880: 59; Dall 
1 885: 280, pi. 1 8, fig. 3; Dall, 1 889: 92, pi 
47, fig. 3; Maury, 1922: 54; Peile, 1926 
88; M. Smith, 1937: 146, pi. 55, fig. 7, pi 
67, fig. 3 [pi. 67 copied from Dall (1 885: pi 
18)]; Perry, 1940: 117, pi. 39, fig. 286 
Broek, 1950: 80; Morrison, 1951b: 8 
Dodge, 1955: 64-68 [history of nomen- 
clature]; Perry & Schwengel, 1955: 197, 
pi. 39, fig. 286; Morris, 1958: 228, pi. 40, 
fig. 14; Coomans, 1958: 103; Morrison, 
1958: 118-124 [habitat]; Nowell-Usticke, 
1959: 88; Holle & Dineen, 1959: 28-35, 
46-51 [shell morphometry]; Golley, 1960: 
152-155 [ecology]; Warmke & Abbott, 
1961: 153 [pi. 28, fig. n is of Melampus 
(Detracia) monile (Bruguière)]; Marcus & 



250 



MARTINS 



Marcus, 1963: 41-52 [early life history]; 
Marcus, 1965: 124-128 [systematicsj; 
Marcus & Marcus, 1965a: 19-82, figs. 
1-18 [distribution, ecology, anatomy]; 
Natarajan & Burch, 1966: 114 [chromo- 
somes]; Scarabino & Maytia, 1968: 276- 
278; Coomans, 1969: 82; Rios, 1970: 
1 38; Vilas & Vilas, 1 970: 91 , pi. 1 0, fig. 21 ; 
Princz, 1973: 183; Morris, 1973: 273, pi. 
74, fig. 11; Abbott, 1974: 332, fig. 4088; 
Humphrey, 1975: 196, pi. 22, fig. 27 [fig- 
ured dorsal view looks very much like 
Melampus (D.) monile (Bruguière)]; Rios, 
1975: 158, pi. 48, No. 764; Emerson & 
Jacobson, 1976: 192, pi. 26, fig. 26; 
Berry, 1977: 181-226; Cosel, 1978: 215; 
Rosewater, 1981; 161; Rehder, 1981: 
646, fig. 362; Heard, 1982: 20, fig. 15; 
Mahieu, 1 984: 31 4; Jensen & Clark, 1 986: 
457, figured. 

Melampus (Tralia) olivula (Küster). H. & A. Ad- 
ams, 1854: 11. 

Melampus olivula (Küster). Pfeiffer, 1854b: 
147; Pfeiffer, 1856a: 23; Pfeiffer, 1876: 
304; Lange de Morretes, 1949: 122; 
Morrison, 1951b: 8. 

Melampus biplicatus (Deshayes). Pfeiffer, 
1856a: 21; Pfeiffer, 1876: 303. 

Melampus caffeus (Lamarck) (Linnaeus). Dali, 
1883: 322 [misspelling]. 

Melampus caffeus (Linnaeus). Simpson, 
1889: 68 [misspelling]. 

Melampus coffea, var. microspira Pilsbry, 
1891: 320 [Progreso, Yucatán, Mexico; 
holotype ANSP 61471 (Fig. 221)]. 

Melampus (Melampus) со ff eus (Linnaeus). 
Dali & Simpson, 1901:368, pl. 53, fig. 13; 
Thiele, 1931; 467; Zilch, 1959: 65, fig. 
21 1 ; Vokes & Vokes, 1 983: 6. pl. 22, fig. 
13. 

Melampus coffeus coffeus (Linnaeus). C.W. 
Johnson, 1934: 159. 

Melampus (Melampus) coffea (Linnaeus). Al- 
tena, 1975: 86, pl. 8, fig. 8; Gibson-Smith 
& Gibson-Smith, 1982: 116, fig. 1. 



Description: Shell (Figs. 218-233) to 23 mm 
long, ovate-conic, solid, shiny to dull, whitish 
to dark brown with olive tones, sometimes 
monochrome, rarely with irregular axial mark- 
ings, generally with as many as five olive 
green to brown bands on body whorl, the one 
just below shoulder markedly consistent; 
pinkish to dark brown patch usually covering 
tip of columella and columellar tooth. Umbil- 
ical excavation visible in large specimens. 



Spire low, whorls nine to 12, flat; the first 
three and one-half to four whorls of teleo- 
conch dark brown, spirally pitted; four rows 
of pits in first whorl, gradually disappearing at 
a rate of about one a whorl; remaining whorls 
smooth or marked with very fine superficial 
cords, not related to the preceding pits; body 
whorl about 90% of total length, cahnate at 
shoulder, near its broadest point, smooth ex- 
cept around columella, which is striated. Ap- 
erture narrow, broadening anteriorly, subax- 
ial, averaging 93% of body whorl length; 
inner lip with small, oblique columellar tooth, 
two parietal teeth, posterior one moderately 
strong, perpendicular to columellar axis, an- 
terior one minute, sometimes fused with pos- 
terior one, sometimes absent; rarely with ad- 
ditional parietal denticles above posterior 
parietal tooth; outer lip sharp, with 13 to 18 
even, white internal riblets not reaching edge. 
Inner whorls greatly resorbed, partition ex- 
tending into only half of body whorl (Fig. 225). 
Protoconch smooth, translucent, brownish 
(Figs. 230-233). 

Radula (Figs. 234-251) with formula [32 + 
(1 + 26) + 1 +(26 + 1) + 32] X 113. Base of 
central tooth approximately same width as 
that of lateral teeth, triangular, laterally con- 
stricted on first third; crown small, posterior 
edge with medial depression; mesocone 
small, sharp; ectocones very small or absent. 
Lateral teeth 20 to 36; crown strong, broadly 
triangular, one-third of total length of tooth; 
irregularities on crown give it tricuspid ap- 
pearance, but distinct endocone or ectocone 
not present. Marginal teeth 28 to 38; meso- 
cone large, triangular, pointing medially; en- 
docone small, sometimes divided into as 
many as five small denticles that can give a 
serrated appearance; ectocone appearing as 
serrate edge in crown of first marginal tooth; 
denticles becoming distinct around seventh 
to tenth marginal tooth; from about 20th mar- 
ginal tooth onward, ectocone becomes 
cteniform with as many as eight denticles. 

Animal (Fig. 252) brownish, mottled to uni- 
form black. Mantle skirt broad, with numer- 
ous mucous cells; right and left margins pos- 
teriorly fused to form pointed lappet of 
posterior aperture canal. Palliai cavity deep, 
not covering entire body whorl, opening to 
outside through semicircular pneumostome 
on right side of mantle skirt. Rectum delimits 
right side of palliai cavity; bilobed anal gill 
flanking rectum just posterior to anus. Long, 
weakly developed hypobranchial gland just 
to left of rectum. Kidney contiguous with hy- 



WESTERN ATLANTIC ELLOBIIDAE 



251 




FIGS. 230-233. Melampus (M.) coffeus, lateral and top views of spire and protoconch. (230, 231) South 
Mastic Pt., Andros Island, Bahamas. (232, 233) Tucacas, Venezuela. Scale, Fig. 231, 500 ¡im; all others, 
1 mm. 



pobranchial gland, white, long, narrow, with 
incomplete transverse foldings forming lon- 
gitudinal medial atrium; kidney opening pap- 
illose, emptying into mantle cavity just pos- 
terior to dorsal pneumostomal gland. Grayish, 
white-spotted pneumostomal glands in front 
of kidney, one on roof, other on floor of palliai 
cavity. Mantle organ in anterior left corner, 
well developed, dark brown to black. Heart 
transparent, posterior to kidney and mantle 
organ; posterior ventricle gives off short aorta 
that branches anteriorly and posteriorly; an- 
terior aorta large, passing beneath crop, 
crossing to right over columellar muscle and 
under right parietovisceral connective, and 
emptying into large pedal sinus; posterior 
aorta branches to digestive gland, intestine, 
stomach and ovotestis; some blood collects 
in wide circular vein of mantle skirt and passes 
to pulmonary vein that opens into auricle; rest 
of blood passes through kidney and mantle 
organ, joining pulmonary vein at entrance of 
auricle. Stomach (Fig. 253) as in subfamily. 



Reproductive system (Fig. 254) basically 
as described under Melampus s. I.; vagina 
about one and one-half times length of body 
whorl; posterior vas deferens about half the 
length of vagina. 

Nervous system (Fig. 255) having cerebral 
ganglia joined by thick cerebral commissure, 
usually heavily wrapped in connective tissue; 
cerebral commissure shorter than width of a 
single cerebral ganglion. Ten pairs of nerves 
originate on cerebral ganglia; from anterior to 
posterior, they are: large tentacular nerve in- 
nervating tentacles; ocular nerve to eyes; 
peritentacular nerve going to base of tenta- 
cles; anterior labial nerve innervating sides of 
mouth; thicker medial labial nerve with one 
branch to sole of labial palps and two 
branches to lips and right medial labial nerve 
sends a branch to penis (penial nerve); pos- 
terior labial nerve innervating ventral portions 
of mouth; long cerebrobuccal connective; 
thick cerebropedal connective; thin statocyst 
nerve; and thick cerebropleural connective. 



252 



MARTINS 




FIGS 234-242. Melampus (M.) coffeus, radula, Hungry Bay, Bermuda, si 14.1 mm. (234) General view, left 
half. (235, 236) Left lateral teeth. (237, 238) First left marginal teeth. (239) Central and first right lateral teeth. 
(240, 241) Last left marginal teeth. (242) Last right marginal teeth. Scale, Fig. 241 , 500 цт; all others, 50 цт. 



WESTERN ATLANTIC ELLOBIIDAE 



253 




FIGS. 243-250. 



254 



MARTINS 



С 1L 23L Т IM 2М ЗМ 




ЮМ 11М 12М 18М 19М 25М 26М 27М 




FIG. 251. Melampus (M.) coffeus, radula, Mullet 
Key, Florida. Scale 10 цт. 

Buccal ganglia small, joined by short, thin 
buccal commissure from which unpaired 
pharyngeal nerve leaves, embedding into 
buccal bulb just anterior to radular sac; a pair 
of esophageal nerves leave medial anterior 
portion of ganglia, splitting immediately into 
anterior and posterior esophageal nerves, the 
latter running posteriorly on sides of esoph- 
agus; cerebrobuccal connectives securely 
attached to sides of buccal bulb, at which 
they emit a lateral buccal nerve; the salivary 
gland nerve branches off cerebrobuccal con- 
nectives and enters salivary ducts near junc- 
tion with buccal bulb. 

Pleural ganglia small, lacking nerves di- 
rectly associated with them other than cere- 
bropleural, cerebropedal and pleuroparietal 
connectives; thin cutaneous lateropleural 
nerve extends from lower posterior portion of 
pleuropedal connective to lateral mid-foot re- 
gion; left pleural ganglion about 30% of size 
of right pleural ganglion; left pleuroparietal 
connective twice length of right one. 

Parietal ganglia unequal. Left ganglion half 
size of right one, with fewer nerves; mantle 
skirt artery nerve leaving ganglion anteriorly, 
entering mantle skirt on left side, running 
along artery, sending branch into dorsal por- 
tion of mucous gland; thin external palliai 
nerve going to posteroventral section of 



mantle skirt; parietocutaneous nerve with 
branch to origin of posterior left bundle of 
columellar muscle; internal palliai nerve to 
mantle skirt, bifurcating to left side and to 
posteroventral portion. Nerves from right pa- 
rietal ganglion are: external palliai nerve orig- 
inating ventrally near pleural ganglion, cross- 
ing beneath other right parietal nerves and 
ramifying in floor of lung; thick pneumo- 
stomal nerve following floor of pneumostome 
and branching to innervate lips of pneumos- 
tome; medial palliai nerve arising above 
pneumostomal nerve and branching into 
mantle skirt; internal palliai nerve arising 
above pneumostomal nerve and branching 
into mantle skirt; internal palliai nerve, closely 
associated with pneumostomal nerve, going 
to roof of mantle cavity; and aortic nerve in- 
nervating wide aorta. 

Visceral ganglion about same size as right 
parietal ganglion, giving off these nerves: 
thick palliai cutaneous visceral nerve crosses 
from left to right to innervate mantle lappet; 
thinner anal nerve goes to lower pneumos- 
tomal gland and anal region; genital nerve 
gives off thin branch to columellar muscle, 
extends along posterior vas deferens, sends 
branch to albumen and mucous glands and 
continues to ovotestis; and thinner columel- 
lar muscle nerve arises to right of genital 
nerve and penetrates columellar muscle. 

Pedal ganglia united in front by pedal com- 
missure and posteriorly by thin subpedal 
commissure. There are seven pairs of pedal 
nerves: anteromedian pedal nerve goes for- 
ward to mid-ventral foot; anterolateral pedal 
nerve runs laterally and anteriorly; anterior 
and posterior cutaneous pedal nerves go 
midlaterally to wall of foot; posterolateral 
pedal nerve runs posterolaterally; postero- 
median pedal nerve goes to posterior mid- 
ventral section; and posteropedal nerve goes 
to posterior ventral portion of foot. Thick 
cerebropedal and thinner pleuropedal con- 
nectives insert close to each other on anterior 
and lateral margins of ganglion respectively; 
thin statocyst nerve inserts just above cere- 
bropedal commissure; thin left pharyngeal 
retractor muscle nerve originates posterior to 



FIGS. 243-250. Melampus (M.) coffeus, radula. (243) Laguna Rincón, Bahía de Boquerón, Puerto Rico, si 
2.33 mm; central tooth hidden by tricuspid first lateral teeth. (244) Laguna Rincón, Bahía de Boquerón, 
Puerto Rico, si 2.33 mm. (245, 246) Laguna Rincón, Bahía de Boquerón, Puerto Rico, si 3.48 mm. (247-249) 
Shore of Millars Road, New Providence, Bahamas, si 4.63 mm. (250) Left lateral teeth, with articulation of 
medial node of base of one tooth with crown of next tooth. Punta Arenas, Puerto Rico, si 19.9 mm. Scale 
50 |jm. 



WESTERN ATLANTIC ELLOBIIDAE 



255 



upgl 





avd 


aa 


; tcm 


pe 


on 




FIG. 252. Melampus (M.) coffeus, anatomy. Right and anterior sides of mantle cavity cut, roof of lung 
reflected to left; neck incised longitudinally, neck skin reflected laterally; insertion of penial retractor muscle, 
columellar muscle and anterior aorta cut; floor of mantle removed, organs cleaned of connective tissue and 
sligtitly separated. Scale 1 mm. 




FIG. 253. Melampus (M.) coffeus, stomach, Florida. 
Scale 1 mm. 



statocyst nerve, follows the latter forward 
and, halfway, turns posteriorly and inserts in 
radular muscle; wide sheet of connective tis- 




FIG. 254. Melampus (M.) coffeus, reproductive sys- 
tem. Grassy Key, Florida. Scale 1 mm. 

sue wraps connectives associated with pedal 
ganglia, statocyst nerve and proximal portion 
of radular muscle nerve; right pharyngeal re- 
tractor muscle nerve and associated connec- 
tive tissue attach to posterior right side of 
buccal bulb. Round statocyst with numerous 



256 

pmpa pgst pipn 



MARTINS 

pcpn 
acpn 

alpn phmn 
. -'' ampn man 



epic 




ipan\ pnn 



, , . •. > f '\ Clpln , , , v 

piprc pipe epan mpan prg pig ¿pe pin pen \iin 



pn 



cbe 

sgln 
.aoen 
p\ poen 
;\ Ъе 
Vt)hn 

. '^tn 
ptn 



FIG. 255. Melampus (M.) coffeus, central nervous system, Grassy Key, Florida. Scale 1 mm. 



statocones on anterodorsal surface of each 
pedal ganglion. 

Remarks: Dodge (1955) gave a detailed ac- 
count of the nomenclatorial history of Melam- 
pus (M.) coffeus (Linnaeus). The description 
provided by Linnaeus (1 758) was so brief and 
general that it could be applied to almost any 
species of Melampus. The specific charac- 
ters nnentioned were the aperture dentate on 
both sides and conical shell, characters com- 
mon among ellobiid species. A synonymy 
was not given, references to any illustration 
were not cited, and the locality was unknown. 
In his copy of the twelfth edition of the Sys- 
tema Linnaeus added a manuscript reference 
to Lister (1770: fig. 59) (Dodge, 1955). Al- 
though the abbreviation "Barb" [for Barba- 
dos] is written between figures 59 and 60, 
plate 834, of Lister, the sketchy representa- 
tion of the outer lip in figure 59, chosen by 
Linnaeus, suggests a species of the Indo-Pa- 
cific genus Cassidula. Such was the interpre- 
tation of Hanley (1855: 214), who regarded it 
as being Bulimus auhs-felis Bruguière [= Cas- 



sidula aurisfelis] "or some closely allied con- 
gener." Also according to Hanley, Cassidula 
aurisfelis was not present in the Linnaean col- 
lection although Linnaeus asserted that he 
owned the specimen he used for the descrip- 
tion of his Bulla coffea. 

The history of the interpretation of the 
name Bulla coffea exemplifies the confusion 
of the various authors about the identity of 
Linnaeus' species. One of the illustrations 
cited in early works for the Linnaean species 
is a dorsal view of the Auricula Midae non- 
fimbriata, bidens of Martini (1773, 2: 126, pi. 
43, fig. 445). Although Martini's description 
and figure are rather sketchy and inaccurate, 
he cited in synonymy Petiver's (1 770) species 
No. 493, Perslcula barbadensis fasciatus. The 
locality, Barbados, is within the range of the 
species and agrees with Lister's note. Chem- 
nitz [1786, 9(2): 45, figs. 1043, 1044] also il- 
lustrated and described under the name Vo- 
luta coffea Linnaei his concept of Linnaeus' 
species, referring to the tenth and twelfth edi- 
tions of the Systema. Chemnitz criticized 
Martini's illustration as a "small, unimportant 



WESTERN ATLANTIC ELLOBIIDAE 



257 



and unrecognizable figure of the present 
much larger and impressive shell." The 
Chemnitz definition and illustration are 
equally incorrect, however; the former men- 
tions fine transverse striae, the latter closely 
resembles Cassidula aurisfelis (Bruguière, 
1789). An indication that Chemnitz w/as con- 
fused about the true identity of Linnaeus' 
species is the reference to the size. Cassidula 
aurisfelis easily reaches 30 mm whereas 
Melampus (M.) coffeus rarely surpasses 20 
mm in length. 

Probably with the intention of clarifying the 
existing confusion Bruguière (1789) intro- 
duced the name Bullmus coniformis, for 
which he provided a fairly accurate descrip- 
tion. He cited in the synonymy Lister's figure 
59, Linnaeus (1758, 1767) and Martini's fig- 
ure 445. He rejected, however, Chemnitz' 
figure, which shows an apertural view. 

The thirteenth edition of the Systema nat- 
urae (Gmelin, 1791: 3438) also failed to re- 
solve adequately the question of the identity 
of Melampus (M.) coffeus (Linnaeus). Gmelin 
listed Voluta coffea, and the references to the 
synonymy included Lister's figure 59, Fa- 
vanne's (1780) figure H7 [miscited as fig. 47], 
Martini's figure 445 and Chemnitz' figures 

1043, 1044. Two pages before (p. 3436) 
Gmelin introduced Voluta minuta, for which 
he cited the same references to Lister and 
Martini. He described two color patterns, 
dark with two to six white bands, or white 
with four alternating yellow and coffee-col- 
ored bands. These features are not surpris- 
ing, considering the variation in color that 
characterizes the group. Reference to the 
"three ribs on the outer lip" raises doubt 
about the relationship of Voluta minuta to 
Melampus (M.) coffeus, because the latter 
species has many (13-18) riblets inside the 
outer lip. Voluta minuta has been cited fre- 
quently as junior synonym of Melampus (M.) 
coffeus. Given both the impossibility of iden- 
tifying Gmelin's species from the original de- 
scription, and the ambiguity of the illustra- 
tions cited in the synonymy, however, the 
name Voluta minuta of Gmelin must be 
treated as a nomen dubium. 

Röding (1798: 106) introduced the names 
Elloblum Inflammatum and Elloblum barba- 
dense and referred both to Voluta coffea 
(Linnaeus). No locality was given for the 
"Banded Midas ear," Elloblum Inflammatum, 
and the additional references are the Lister 
figure 59 and the Chemnitz figures 1043, 

1044, already discussed and considered in- 



conclusive. The only reference given for Ello- 
blum barbadense was the unidentifiable Mar- 
tini figure 445. Röding did not provide any 
description and, as noted, the references 
given are inconclusive. For this reason, Ello- 
blum Inflammatum and Elloblum barbadense 
are to be considered nomina dubia. 

According to Dodge (1955) Melampus (M.) 
coffeus is not described in the Museum Ulrl- 
cae, and specimens of it are not in the 
Queen's collection at Uppsala. Inspection of 
the type material at the Linnaean Society of 
London revealed a mixed lot of 12 specimens 
representing two species. A label note by S. 
P. Dance from 1963 attributes to Hanley the 
selection of these 12 unmarked specimens. 
Seven specimens are Melampus (D.) monile 
(Bruguière), four represent a smaller form of 
Melampus (M.) coffeus (Linnaeus) (Fig. 219) 
and the twelfth specimen, nearly twice the 
size of any of the others, conforms to Melam- 
pus (M.) coffeus (Linnaeus) of all authors (Fig. 
218). 

With all the inconsistencies in the descrip- 
tions and figures applied by the early authors 
to Bulla coffea Linnaeus, this name, as 
Dodge (1 955: 67) remarked, would be treated 
as nomen dubium were it not for the exis- 
tence in the Linnaean collection of a speci- 
men that must be considered the ostensible 
type. Equally important is the fact that the 
name Melampus (M.) coffeus has been in 
general use since 1854 and to remove this 
well-established name would create unnec- 
essary confusion in the literature. To prevent 
further confusion, the large specimen in the 
LSL (Fig. 218) is herein designated lectotype. 

Another source of confusion was the 
failure of some authors to distinguish be- 
tween Melampus (M.) coffeus (Linnaeus) and 
Melampus (M.) bidentatus Say. The geo- 
graphical ranges of these two species over- 
lap in Bermuda, most of Florida, the Gulf of 
Mexico and the western Greater Antilles. 
Melampus (M.) bidentatus is highly variable, 
sometimes resembling the highest-spired 
Melampus (M.) coffeus in shape, size and 
color. The most distinctive characteristic, as 
noted by Morrison (1958, 1964), is the ab- 
sence of incised lines on the shoulder of the 
body whorl of Melampus (M.) coffeus. This 
characteristic can be used only in individuals 
having more than four whorls. In fact, the first 
three and one-half to four whorls of both spe- 
cies have incised lines and are indistinguish- 
able in this regard (Figs. 230-233). Binney 
(1859) and Tryon (1866) perceived this differ- 



258 



MARTINS 



ence, describing Melampus (M.) coffeus as 
having microscopic revolving lines, as op- 
posed to Melampus (M.) bidentatus, which 
has revolving striae. Lines are very weak 
cords whereas striae are finely impressed 
spiral depressions. The lines in Melampus 
(M.) coffeus are not incised and they do not 
correspond to the continuation of the stria- 
tions or rows of pits on the first whorls. 

Failure to distinguish between Melampus 
(M.) coffeus and Melampus (M.) bidentatus is 
obvious in the work of Holle & Dineen (1959). 
One of their conclusions is the hypothesis 
that Melampus (M.) coffeus and Melampus 
(M.) bidentatus are but subspecies. Natarajan 
& Burch (1966), on the basis of chromosomal 
counts, stated that these species hybridize. I 
doubt, however, that they were dealing with 
both species, but rather with two forms of the 
variable Melampus (M.) bidentatus. The sup- 
posed Melampus coffeus used in their re- 
search was from Jekyll Island, Georgia. In- 
spection of four major museum collections of 
the east coast of the United States failed to 
yield any record of Melampus (M.) coffeus 
north of Florida. It is doubtful, therefore, that 
this species was involved and the suggestion 
that Melampus (M.) bidentatus and Melam- 
pus (M.) coffeus hybridize is probably unten- 
able. 

Deshayes (1 830) introduced Auricula bipli- 
cata, of unknown locality. Beck (1837) re- 
ported Deshayes' species as living in Amer- 
ica and Binney (1859), probably on account 
of Beck's reference to the name biplicata, 
treated Auricula biplicata as a synonym of 
Melampus (M.) bidentatus, without comment. 
In the original description Deshayes (1830: 
91) stressed that his species should not 
be confused with those under the section of 
the Conovules. In comparing Auricula bipli- 
cata with Auricula coniformis (Bruguière) 
[= Melampus (M.) coffeus], Deshayes pointed 
out that, although comparable in size [22 x 12 
mm], his species differed from Bruguière's 
species in color, shape and apertural denti- 
tion. The holotype of Auricula biplicata 
(Fig. 220) lacks the incised grooves on the 
shoulder of the body whorl, characteristic 
of Melampus (M.) bidentatus. The uniform 
brownish color, the slender shape, the 
strong, whitish posterior parietal tooth and 
the greatly reduced anterior parietal tooth are 
well within the range of variation that I have 
observed in Melampus (M.) coffeus. I col- 
lected in Florida specimens that conform 
with Deshayes' species. I have designated 



herein Barbados as the type locality for Au- 
ricula biplicata Deshayes to avoid confusion 
with a large form of Melampus (M.) bidenta- 
tus, also found in Florida, which Pfeiffer 
(1853b) described as Melampus gundlachi 
(Fig. 271). 

Melampus olivula (Küster) is a Brazilian 
morph of Melampus (M.) coffeus character- 
ized by the absence of the first parietal tooth 
(Fig. 228). Although Küster (1844: 33) referred 
to an alleged publication by Moricand in 
"Memoir de la Société de Genève. VIN", I 
failed to see such a reference in the place 
indicated. Accepting Pfeiffer's (1856a) au- 
thority, who attributed Auricula olivula to 
Moricand "ex citationibus auctorum," one 
can conclude that Mohcand's publication of 
the name is doubtful or obscure, and Küster 
(1844) is to be credited for its introduction. 

As pointed out under the remarks for the 
subgenus, the radular morphology of Melam- 
pus changes considerably during the early 
growth of the animal (Figs. 243-249). Among 
the most noticeable differences are the wide 
base of the central tooth bearing conspicu- 
ous nodes on the inner edge of the arms and 
the clearly tricuspid first lateral tooth with ec- 
tocone and endocone that becomes serrated 
in larger juveniles. In juveniles, as in adults, 
the transitional tooth is characterized by a 
shortening of the base and the presence of 
an ectocone. The marginal teeth also have an 
endocone. The number of cusps on the ec- 
tocone can vary from row to row in the same 
positional tooth. 

A unique feature of the Melampinae is the 
mantle organ. This squarish, black structure 
was first mentioned by Koslowsky (1933: 
178) for Melampus boholensis H. & A. Ad- 
ams, and by Marcus & Marcus (1 965a: 31 ) for 
Melampus (M.) coffeus. Although of unknown 
function, this highly vascularized organ prob- 
ably is excretory or lymphatic, according to 
the latter authors. 

Another structure, here called the bilobed 
anal gill, was described by Koslowsky (1933) 
and by Marcus & Marcus (1965a) as a pair of 
anal glands. It consists of two small, pro- 
fusely ciliated tubular structures flanking the 
anus and isolated from the palliai cavity. Ac- 
cording to Marcus & Marcus (1965a: 38) this 
structure, consisting of epithelial cells and 
subepithelial secretory cells, probably se- 
cretes some mucilaginous substance that 
helps in holding the fecal pellets together and 
in lubricating the anal groove. Renault (1966) 
described the same structure in Cassidula la- 



WESTERN ATLANTIC ELLOBIiDAE 



259 



brella Deshayes, but considered it a gill. In 
the Pythiinae, to which Cassidula belongs, 
and in the Pedipedinae I observed it to be a 
single, well-developed, highly folded struc- 
ture, closely resembling a gill. Renault noted 
that this structure is at the bottom of a de- 
pression in the mantle-skirt groove and con- 
cluded that such a depression is comparable 
to a reduced palliai cavity, seen in the ontog- 
eny of some pulmonates and retained in 
adult ellobiids. Although not denying its glan- 
dular character, I am inclined to consider this 
structure in Melampus (M.) coffeus as a gill 
because of its homology with identical or- 
gans in the Pedipedinae and Pythiinae. 

The connectives of the visceral nerve ring 
are short, but readily identifiable and of un- 
equal length. In this respect Marcus & Mar- 
cus' illustration (1965a, pi. 2, fig. 7) of the 
central nervous system of Melampus (M.) 
coffeus is inaccurate in not showing evidence 
of those connectives, a condition never 
found in the ellobiids. 

Habitat: Melampus (M.) coffeus, an inhabit- 
ant of mangroves, lives at and above the 
high-tide mark but can also occur intertidally, 
commonly gathering on mangrove roots and 
propagules above water level at high tide, but 
descending to the muddy ground at low tide. 
They prefer shady places (Marcus & Marcus, 
1965a) and seem to be more active at night 
(Golley, 1960). 

Range: Bermuda; Florida to West Indies; 
Gulf of Mexico, Central America south to Bra- 
zil (Fig. 256). Scarabino & Maytia (1968) re- 
ported this species from Uruguay, where four 
beach specimens were collected; the authors 
suggested that they might have been carried 
by currents from nearby Brazil. 

Specimens Examined: FLORIDA (ANSP 
56829): Indian River (USNM 758220); S of 
Sebastian Inlet (MCZ 143993); Coconut 
Grove (MCZ 291328, 291330; USNM 
603112); Miami (USNM 700802); Biscayne 
Bay (USNM 6031 16); Brickell Hammock, Bis- 
cayne Bay (MCZ 291325); Homestead (MCZ 
291097); Card Sound (ANSP 84403); Turner 
River, Card Sound (ANSP 93430); Barnes 
Sound (MCZ 291095); Middle Key (USNM 
338339); McGinty Key (ANSP 139532); Key 
Largo (ANSP 194009; MCZ 246700, 291324; 
USNM 529249, 603118); Tavernier (ANSP 
325296; MCZ 201659); Tavernier Creek 
(USNM 667400; A.M.); Tavernier Key (USNM 




FIG. 256. Melampus (M.) coffeus, geographic dis- 
tribution. Open circle, locality from literature. 



492563); Snake Creek (MCZ 291012); Snake 
Key (ANSP 1054); Plantation Key (MCZ 
199340, 291016; A.M.); Windley Key (USNM 
603103); Indian Key Fill (A.M.); Lignumvitae 
Key (ANSP 156326); MCZ 75605); Mate- 
cumbe Key (USNM 822252); Lower Mate- 
cumbe Key (USNM 700764); Rabbit Key 
(ANSP 88135); Long Key (MCZ 176170; 
A.M.); Grassy Key (MCZ 201673; A.M.); 
Crawl Key (MCZ 291020; A.M.); Key Vaca 
(MCZ 201672); Marathon (MCZ 153253); 
Knight Key (A.M.); Bahia Honda Key (ANSP 
89551 ;USNM 269777b); No Name Key (MCZ 
142470); Little Pine Key (USNM 681643); Big 
Pine Key (ANSP 89552; MCZ 201 651 ; USNM 
597455; A.M.); Ramrod Key (MCZ 291021); 
Pavilion Key (ANSP 93431); Pelican Key 
(MCZ 3967; USNM 39829); Key West (MCZ 
201666; USNM 60754, 668244); Marquesas 
Key (ANSP 73711); Mangrove Key (ANSP 
365478); Flamingo Key (ANSP 294311; MCZ 
235501, 275576, 291098; USNM 672441) 
Cape Sable (ANSP 56825; USNM 603117) 
East Cape, Cape Sable (MCZ 291017) 
Sandy Key (USNM 603121); Lossman River 
(ANSP 132368); Everglades City (MCZ 
291096); Seminole Point (ANSP 105431); 
Horr's Island, Ten Thousand Islands (USNM 
381325); Fakahatchee Key (ANSP 88139); 



260 



MARTINS 



Royal Palm Hammock (MCZ 257250; USNM 
492561); Marco Island (MCZ 201687, 
291011; USNM 381332); Blue Hill Island, 
near Goodland Point (ANSP 88134); Little 
Marco (ANSP 93429); Gordon Pass (USNM 
603098); Naples (MCZ 178104, 201661; 
USNM 667406); Bonita Springs Beach (MCZ 
201680, 291015); Bonita Beach (USNM 
334075); Cayo Tuna, S. Carlos Bay (ANSP 
106299); Carl E. Johnson Park, Little Carlos 
Pass (A.M.); Mound Key, 2 km N of south end 
of Estero Island (MCZ 201657); Dog Key, 1.5 
km NW of middle of Estero Island (MCZ 
201648); Starvation Key (ANSP 130057); Fort 
Myers (ANSP 183181); Punta Passa (ANSP 
45075, 56826, 140849; MCZ 84097, 291018 
USNM 37601, 513900, 492573, 700853 
A.M.); Sanibel Island (ANSP 91378, 170651 
MCZ 13702, 55773, 201655, 291024; USNM 
61 1 799); Wulfert, Sanibel Island (MCZ 1 3703, 
13803); Pine Island (ANSP 93387); Pineaire, 
Pine Island (MCZ 291023); Bokeelia (MCZ 
291025; A.M.); Captiva Island (MCZ 291013; 
USNM 513901); Blind Pass, Captiva Island 
(MCZ 201658); Boca Grande, Gaspahlla Is- 
land (ANSP 142272); Little Gaspahlla Island 
(ANSP 131405); Punta Gorda (ANSP 45076); 
Charlotte Harbor (USNM 592308); Nokomis 
(ANSP 180747); Siesta Key (USNM 669348); 
Sarasota (MCZ 201679; USNM 30625, 
487314a); 4.5 km N of Sarasota (ANSP 
294315); Long Boat Key (MCZ 201686); be- 
tween Palma Sola and Cortez (MCZ 291 01 4); 
Palmetto (A.M.); Manatee River (ANSP 
56832; MCZ 3968, 201664; USNM 492566); 
Big Bend Road [Rt. 672] (A.M.); Tampa Bay 
(MCZ 55757, 70569, 201645, 201654, 
201664; USNM 37602, 73210, 193362, 
196349a, 504481, 711484); Small Island 
(MCZ 91358); Mullet Key (ANSP 76699; 
USNM 652406; A.M.); Tierra Verde (MCZ un- 
catalogued); Shell Key (USNM 466206, 
466288a); key 2 km S of Pass-a-grille (MCZ 
56177); Pass-a-ghlle (ANSP 148522; MCZ 
138939, 162640); Bird Key (ANSP 134318; 
MCZ 71009, 71595, 104946; USNM 36896, 
37600); Terra Ceia (MCZ uncatalogued; 
USNM 124285); Pinellas Point (MCZ uncata- 
logued); St. Petersburg (USNM 341721a, 
466195, 663066); SE of Gulfport (MCZ 
201665); Gulfport (MCZ 88789); Bocea Key 
(USNM 75409); Boca Ciega Bay (ANSP 9568; 
MCZ 291329); Sand Key (ANSP 128525); 
Clearwater Island (ANSP 9354, 176363; MCZ 
1 05461 ; USNM 61 1 786); island in Clearwater 
Bay (ANSP 149851); Anclote River (A.M.); 
Cedar Key (ANSP 362803; MCZ 201660; 



USNM 27918). BERMUDA (ANSP 158807; 
USNM 11421, 94432a, 173642, 228686): in- 
let E of biological station, St. George's (MCZ 
64705); Hungry Bay (ANSP 85712; MCZ 
24247; A.M.); BAHAMA ISU\NDS (ANSP 
56830); GRAND BAHAMA ISU\ND (ANSP 
374525): Gold Rock Creek (ANSP 369339); 
Running Mon Canal (ANSP 369778); Eight 
Mile Rock (ANSP 173255); Hawksbill Creek 
(ANSP 176351; MCZ 116679); GREAT 
ABACO ISLAND (ANSP 362802, 362804; 
MCZ 201683; USNM 492564, 492591): Witch 
Point (ANSP 299482); Bootle Bay (ANSP 
371879); Cherokee Sound (MCZ 133101); 
BIMINI ISLANDS: Alicetown, North Bimini 
(MCZ 144186); BERRY ISLANDS (MCZ 
291332); ANDROS ISLAND (USNM 492572): 
South Mastic Point (A.M.); Stafford Creek 
(ANSP 189566); Mangrove Cay (ANSP 
94525; MCZ 24137, 24138; USNM 269861, 
269968b); Lisbon Point, Mangrove Cay 
(USNM 269599); Linder Key (USNM 
270483a); NEW PROVIDENCE ISLAND 
(ANSP 184850; MCZ 85768): Nassau (USNM 
160765, 467072, 568412); Old Fort (MCZ 
1 07792); Dick's Point (MCZ 1 07797, 113101, 
291333); Adelaide (USNM 603873); Millars 
Sound (A.M.); Millars Road (A.M.); Bonefish 
Pond (USNM 618597; A.M.); Fox Hill, South 
Beach (MCZ 107770); ELEUTHRA ISLAND: 
Schooner Cays (ANSP 359332); Millars 
Beach (ANSP 359351); ROYAL ISLAND 
(MCZ uncatalogued; USNM 468114); CAT 
ISLAND (ANSP 173256): Russell Creek 
(ANSP 173260; MCZ 63384); Orange Creek 
(ANSP 173254; MCZ 63385); Arthurstown 
(ANSP 173661; MCZ 107832); Dumfries 
(MCZ 107752); EXUMA CAYS: Hog Cay 
(ANSP 285755); SAN SALVADOR ISLAND 
Riding Rock (USNM 36031 1); LONG ISLAND 
Salt Pond, Clarencetown (ANSP 189565 
MCZ 113099; USNM 589832, 590247) 
Brett's Hill (MCZ 113336, 142299); Glenton's 
(ANSP 173253; MCZ 113100; Cape Sta. 
Mana (MCZ 113329). CUBA (ANSP 56791; 
USNM 10967, 59724, 121518, 492569, 
492581): Bahia de Santa Rosa (USNM 
492556, 492568); Cape Cajón (USNM 
492571a); Los Arroyos (USNM 492558); 
Cayo Rapado (MCZ 201652); Dimas (USNM 
492559a); Bahia Honda (USNM 492560); Ma- 
riel (MCZ 131922; USNM 169938); Mahanao 
(ANSP 77006; MCZ 131953); Rio San Juan 
(MCZ 127825); Cayo Cristo (MCZ 291321); 
Cárdenas (MCZ 87886); Rio Yumuri (ANSP 
87920, 167219; MCZ 83311, 131913, 
131941, 201684); Cayo de las Cinco Léguas 



WESTERN ATLANTIC ELLOBIIDAE 



261 



(ANSP 158050); Rancho Veloz, Sagua la 
Grande (MCZ 201682); Caibarién (MCZ 
131914, 131920, 131940); Cayo Francés 
(MCZ uncatalogued); Muelles (MCZ 131915); 
Cayo Salinas, Buena Vista Bay (MCZ 
201681); Cayo Conuco (MCZ uncatalogued); 
Isla de Cobos (MCZ uncatalogued); Punta 
Alegre (ANSP 149212); Isla Tuhgano (MCZ 
uncatalogued); Terraplén, Isla Turigano 
(USNM 385661); S of Central Ramon (USNM 
391797); Gibara (USNM 381469, 603096); 
Bañes (MCZ 59623); Penon el Fraile, Fraile, 
Santa Cruz del Norte (USNM 807577); Playa 
Cajio, Güira del Melena (USNM 803401); 
Guantánamo Bay (MCZ 92675); Santiago 
(USNM 373225, 603114); Tarallones de 
Arena, near Santiago (ANSP 182935); Rio 
Cauto (USNM 682787); Santa Cruz del Sur 
(MCZ 131919, 201662); Finca, Sabanalmar 
(MCZ uncatalogued); Cíenfuegos Bay (ANSP 
106093); Alto del Caracol (ANSP 222629); 
Cienfuegos Bay, 1 km E of La Milpa (MCZ 
uncatalogued); Cayo Blanco (ANSP 157942); 
Batabanó (ANSP 93714; USNM 603115); La 
Coloma (MCZ 84884, 131949); Punta de 
Llana (MCZ 201668); Isla de Pinos (MCZ 
48079, 48080). JAMAICA (ANSP 56822; MCZ 
291233, 291318, 291322; USNM 94743, 
492562, 492570): Green Island Harbor 
(USNM 440805); Fort Clarence (USNM 
433433); Montego Bay (ANSP 329154; MCZ 
17452); Port Morant (USNM 375739); Cow 
Bay (USNM 440974); Kingston (USNM 
442610); Palisadoes (USNM 442466a); Port 
Royal (USNM 395452c, 427004, 442268); 
Hunt's Bay (USNM 441673); Rock Fort 
(USNM 374232); Phillipsfield (USNM 
402222); Old Harbor (441009); Portland 
(USNM 375680); near Portland Light, Port- 
land Hills (MCZ uncatalogued); Little River 
(USNM 128066); Great Goat Island (ANSP 
344216); Little Goat Island (MCZ 291326); 
Black River (USNM 441356); Savanna la Mar 
(MCZ uncatalogued). HAITI: Fort Liberté 
(USNM 426365); St. Louis (USNM 439390); 
Morne Rouge (USNM 402680, 402715); Go- 
nave Island (MCZ 82119; USNM 492531); 
Port-au-Prince (MCZ 183920; USNM 
403109, 403408, 440460, 440610, 442923); 
Miragoane (MCZ 82072); Anse-à-Maissons, 
Grand Cayamite (MCZ 82100); île-à-Vache, 
Soulette Bay (USNM 439191, 442850); Tor- 
beck (USNM 383068, 403363, 439667, 
439695b); Les Cayes (USNM 439742a); 
Aquin (USNM 367358, 402839, 403255, 
403561, 440163); Bizoton (USNM 439832). 
DOMINICAN REPUBLIC: Monte Cristi (MCZ 



57752, 291334); 19 km E of Monte Cristi 
(USNM 471542); Sanchez (USNM 307261); 
Rio Tapion, Puerto Libertador (USNM 
618639); Puerto Plata (MCZ 90785, 291317, 
291320); Santa Bárbara de Samaná (ANSP 
173257; MCZ 57754); Sanchez (ANSP 
173252; MCZ 57338); Isla La Matica, Playa 
Boca Chica, E of Santo Domingo (R.B.). PU- 
ERTO RICO: San Juan (USNM 161160, 
169885); Cayo Maguey (MCZ uncatalogued); 
Cabo Rojo lighthouse (MCZ 2421 79); Laguna 
Rincón (A.M.); Boquerón Beach (A.M.); Pu- 
erto Real (A.M.); Punta Arenas (A.M.); La Par- 
guera (USNM 622804); Santurce (ANSP 
175624); Piñones (A.M.); Culebra Island 
(USNM 360536). VIRGIN ISLANDS: ST. 
THOMAS (ANSP 56824, 56827; MCZ 89651, 
291319; USNM 6363, 6385a): Benner Bay 
(USNM 702725). ST. JOHN'S (MCZ uncata- 
logued). TÓRTOLA (USNM 6484). ANEGADA 
ISLAND (ANSP 249494; MCZ 229004). ST. 
CROIX (ANSP 56831): Altons Lagoon (USNM 
621394); Salt River (MCZ 110325). LESSER 
ANTILLES: ST. MARTIN'S (ANSP 56821). 
ANTIGUA (ANSP 109156; USNM 215049); 
Fitches Creek (USNM 809739). GUADE- 
LOUPE (MCZ uncatalogued). MARTINIQUE 
(MCZ 56464): between Le Vauclin and Le 
François (ANSP 253289; MCZ 229358). BAR- 
BADOS (MCZ 148628). TOBAGO: Pigeon 
Point (USNM 682273). TRINIDAD: S of Sho- 
ran Site (USNM 608786); Caroni Swamp 
(MCZ uncatalogued); Blue River (R.B.). 
CURAÇAO: Schotteghat, near Willemstad 
(ANSP 133971). CARIBBEAN ISLANDS: 
GRAND CAYMAN ISLAND: 5 km N of George- 
town (ANSP 209765). OLD PROVIDENCE IS- 
LAND (USNM 687818): N of Ironwood Point 
(ANSP 313209; USNM 678832, 678833; MCZ 
270624). MEXICO: Tampico (USNM 219997); 
Vera Cruz (USNM 769426); Rio Vinasco, Vera 
Cruz (USNM 675266); Tuxpan, Vera Cruz 
(MCZ uncatalogued); SE of Tuxpan, Vera Cruz 
(USNM 675271); Mandinga Lagoon, Vera 
Cruz (USNM 791711); Boca del Rio, Vera 
Cruz (MCZ 155429); Isla de Carmen (USNM 
809096); Ciudad del Carmen (USNM 70291 0); 
Rio Champotón (MCZ 59747); Silam (ANSP 
61470); Progreso (ANSP 61469, 61471); 
Rio Lagartos (USNM 618635); Isla Cancún, 
Quintana Roo (ANSP 285520); N end of 
Ascension Bay, Quintana Roo (USNM 
736142, 736691, 738632); Allen Point, 
Ascension Bay, Quintana Roo (USNM 
736695, 736892). BELIZE: Ambergris Cay 
(ANSP 284797); Belize (ANSP 294323); Bo- 
tanical Garden, Belize (USNM 426007); 



262 



MARTINS 



Blackadore Cay (ANSP 282031); Robinson 
Point (ANSP 281579); N of Punta Gorda 
(ANSP 282494). GUATEMALA: Puerto Barrios 
(MOZ 88877). NICARAGUA: Wounta (ANSP 
97591; USNM 181854); Wounta River, near 
Wounta (MCZ 14804); 16 km S of Wounta 
(MCZ 137227). PANAMA (USNM 46182): 
Galeta Island (USNM 703195, 732922, 
732949); Toro Point, Limon Bay (USNM 
732885); Colón (ANSP 107258; MCZ 45058); 
Porto Bello (USNM 21 81 73). COLOMBIA: Sa- 
banilla (USNM 103175); Cartagena (MCZ 
192431); Coveñas, Bolívar (USNM 364336). 
VENEZUELA (MCZ 291327): S of Porlamar, 
Isla Margarita (ANSP 240007; USNM 707796); 
Punta Mangle, ESE of Punta Piedras, Isla Mar- 
garita (MCZ 273661 ); La Orchila Island (USNM 
656031); Carenero (784775); Tucacas (A.M.). 
GUYANA: Demerara (MCZ 177296). SURI- 
NAME: 16 km WNW of Paramaribo (MCZ un- 
catalogued); Nickehe Strand, Zeedijk (MCZ 
uncatalogued); Bigisanti (USNM 635225). 
BRAZIL: Boa Viagem (MCZ 219130); Uru- 
majó, Bragança, Para (ANSP 244096); Praia 
de Búzios, 20 km S of Natal, Rio Grande do 
Norte (ANSP 300442); Praia Upanema, Areia 
Branca, Rio Grande do Norte (ANSP 300320); 
Rio Pirangi (ANSP 300343); Baia (AMNH 
22434; USNM 119506,157674, 465525); Vic- 
toria (MCZ uncatalogued); Rio de Janeiro 
(ANSP 56828; MCZ 89650); Pinheiro Island, 
Rio de Janeiro (USNM 598337). ATLANTIC 
ISLANDS: FERNANDO NORONHA (MCZ un- 
catalogued). 



Melampus (Melampus) bidentatus 

Say, 1822 

Figs. 257-289 

Melampus bidentatus Say, 1822: 245 [East 
Florida, herein restricted to mouth of St. 
John's River; type material presumed lost 
(Baker, 1964); neotype herein designated 
USNM 859014 (Fig. 257)]; Jay, 1839: 59; 
H. & A. Adams, 1 854: 1 0; Pfeiffer, 1 854b: 
147; Pfeiffer, 1856a: 45; Say in Binney, 
1858: 84; Binney, 1859: 156, pi. 75, fig. 
23; Binney, 1860: 4; Binney, 1865: 10, 
figs. 11,12; Tryon, 1866: 8, pi. 18, fig. 5; 
Gould, 1870: 467, fig. 721; Binney & 
Bland, 1870: 286, fig. 7 [radula figured]; 
Pfeiffer, 1 876: 316; Nevill, 1 879: 219; Dall, 
1 883: 322; Whiteaves, 1 901 : 207; Morse, 
1921 : 21 , pi. 7, fig. 46, pi. 9, figs. 46, 46a 



[external anatomy and morphology] 
Peile, 1926: 88; Pilsbry, 1927: 125-126 
Hausman, 1932; 541-545 [ecology] 
Hausman, 1936: 127; M. Smith, 1937 
146, pi. 55, fig. 11, pi. 67, fig. 12 [pi. 67 
copied from Dall (1885: pi. 18)]; Morton, 
1955c: 127-168 [anatomy, evolution]; 
Holle & Dineen, 1 957: 90-95 [life history]; 
Morrison, 1958: 118-124 [habitat]; Mor- 
ris, 1958: 40, fig. 15; Holle & Dineen, 
1959: 28-35, 46-51 [shell morphometry, 
taxonomy]; Baker, 1964: 151; Russell- 
Hunter & Brown, 1964: 143; Russell- 
Hunter & Meadows, 1965: 409 [physiol- 
ogy]; Russell-Hunter &Apley, 1966, 392- 
393 [early life history]; Apley et al. 1967: 
455-456 [annual reproductive turnover]; 
Coomans, 1969: 82; Apley, 1970: 381- 
397 [life history]; Jacobson & Emerson, 
1971: 64, text fig.; Russell-Hunter et al., 
1 972: 623-656 [early life history]; Grandy, 
1972: 106-109 [winter distribution]; Mor- 
ris, 1973: 273, pi. 74, fig. 8; Abbott, 1974: 
331 , fig. 4087; Lesser et al., 1 976: 69-77 
[population density]; Emerson & Jacob- 
son, 1976: 192, pi. 26, fig. 25; Orton, 
1976: 1-57 [ecology]; Andrews, 1977: 
181, figured [common name coffee 
Melampus erroneously applied]; Price, 
1977: 295-312 [central nervous system]; 
Fitzpatrick & Sutherland, 1978: 23-28 
[population density]; Moffett, 1979: 306- 
319 [locomotion]; Andrews, 1981: 77, 
text fig.; Rehder, 1981: 645, fig. 361; 
Heard, 1982: 19, fig. 15; Moffett, 1983: 
950; Ridgway, 1983: 950; Thompson, 
1 984: 44-53 [diet]; Jensen & Clark, 1 986: 
457, figured. 

Melampus bidentatus var. lineatus Say, 1 822: 
246 [Coasts of Maryland and New Jer- 
sey, herein restricted to Bivalve, New 
Jersey, type material presumed lost 
(Baker, 1964); neotype herein desig- 
nated USNM 859013 (Fig. 259)]; Say in 
Binney, 1858: 85; Pfeiffer, 1854b: 147; 
Pfeiffer, 1856a: 46. 

Melampus obliquus Say, 1822: 377 [South 
Carolina; type material lost (Binney, 
1859)]; Pfeiffer, 1854b: 147; Pfeiffer, 
1856a: 30; Say in Binney, 1858: 27; Bin- 
ney, 1860: 4; Pfeiffer, 1876: 306; 
Mazyck, 1913: 2. 

Auricula comea Deshayes, 1830: 90 [New 
York; location of type unknown]; Jay, 
1839: 59. 

Melampus (Melampus) lineatus Say. Beck, 
1837: 107. 



WESTERN ATLANTIC ELLOBIIDAE 



263 



Melampus (Melampus) obliquus Say. Beck, 
1837: 107. 

Melampus (Melampus) corneus (Deshayes). 
Beck, 1837: 107. 

Auricula bidentata (Say). Gould, 1841: 197, 
fig. 130; De Kay, 1843: 57, pl. 5, figs. 92, 
1-3; Küster, 1844: 41, pl. 6, figs. 7-11. 

Auricula jaumei Mittré, 1841: 67 [Hampton, 
Virginia; location of type unknown]. 

Auricula obliqua (Say). De Kay, 1843: 58. 

Melampus lineatus Say. Gray, 1847a: 179 
Dall, 1885: 282, pl. 18, figs. 9, 12; Dall 
1889: 92, pl. 47, figs. 9, 12; Apgar, 1891 
181, figs. 46-48; Mazyck, 1913: 2; C.W 
Johnson, 1915: 178; Maury, 1922: 55 
C.W. Johnson, 1934: 159; Webb, 1942 
pl. 11, fig. 20; La Rocque, 1953: 262 
Coomans, 1958: 103; Bousfield, 1960 
14, pl. 1, fig. 10; Coomans, 1962: 90 
Baker, 1964: 152; Baranowski, 1971 
143. 

Melampus corneus Stimpson. Stimpson, 
1851: 51; Porter, 1974: 301. 

Melampus gundlachi Pfeiffer, 1853b: 126 
[Cayo Blanco, Cuba: location of type un- 
known]; Pfeiffer, 1854a: 147; Pfeiffer, 
1856a: 20; Pfeiffer, 1876: 303: Arango y 
Molina, 1880: 59; A.E. Smith, 1884: 277; 
Crosse, 1890: 258; Kobelt, 1900: 229, pl. 
29, figs. 1, 2; Pilsbn/, 1900b: 504; Mor- 
ton, 1955c: 9; Holle & Dineen, 1959: 28- 
35, 46-51. 

Melampus redfieldi Pfeiffer, 1 854a: 1 1 2 [Ber- 
muda; location of type unknown]; Pfeif- 
fer, 1854b: 147; Pfeiffer, 1856a: 33; Bin- 
ney, 1859: 170; Pfeiffer, 1876: 308; 
Kobelt, 1900: 232, pl. 29, figs. 8, 9; Pils- 
bry, 1900b: 504. 

Melampus 7 jaumei (Mittré). Pfeiffer, 1854b: 
147; Pfeiffer, 1856a: 25. 

Melampus bidentatus var. borealis "Conrad" 
Pfeiffer, 1856a: 46 [Georgia; type in 
Cuming collection, fide Pfeiffer, not 
found at BMNH]. 

Auricula gundlachi {Pie'iiier). Reeve, 1877, pl. 
6, fig. 50. Non Gassies, 1869. 

Auricula redfieldi [РЫ^ег]. Reeve, 1877, pl. 7, 
fig. 52. 

Auricula bidenta (Say). Reeve, 1877, pl. 7, fig. 
54 [error for bidentata, corrected in the 
Index]. 

Melampus spiralis "Pfeiffer" Melvill, 1881: 
155-173 [misidentification]. Non Pfeiffer, 
1855. 

Melampus coffeus var. gundlachi Pfeiffer. 
Davis, 1904: 126, pl. 4, fig. 9; Maury, 
1922: 55; Peile, 1926: 88. 



Melampus coffeus var. redfieldi Pfeiffer. 
Davis, 1904: 126, pl. 4, fig. 10; Peile, 
1926: 88. 

Melampus coffeus var. bishopi Davis, 1904: 
127, pl. 4, fig. 13 [Bermuda; lectotype 
selected by Baker (1964) ANSP 86925 
(Fig. 262)]. 

Melampus coffeus var. verticalis Davis, 1904: 
127, pl. 4, fig. 12 [Bermuda; lectotype 
selected by Baker (1964) ANSP 86927 
(Fig. 263)]. 

Melampus coffeus var. alternatus Davis, 
1904: 127, pl. 4, fig. 11 [Bermuda; lecto- 
type selected by Baker (1964) ANSP 
86926 (Fig. 264)]. 

Melampus coffeus gundlachi Pfeiffer. C.W. 
Johnson, 1934: 159; Perry, 1940: 177. 

Melampus bidentatus corneus (Deshayes). 
Morrison, 1951b: 8. 

Melampus bidentatus lineatus Say. Morrison, 
1951b: 8; Burch, 1960a: 177-208, pl. 1, 
fig. 1 , pl. 4, fig. 62 [chromosomes]; Burch, 
1960b: 454, fig. 5 [chromosomes]; Nat- 
arajan & Burch, 1966: 111, figs. 8, 13 
[chromosomes]. 

Melampus bidentatus bidentatus Say. Morri- 
son, 1951b: 8; 

Melampus bidentatus redfieldi Pfeiffer. Mor- 
rison, 1951b: 8 

Melampus (Micromelampus) bidentatus Say. 
Morrison, 1959: 25. 

Melampus bidentus Say. Porter, 1974: 300 
[error for bidentatus]. 

Melampus (Melampus) bidentatus Say. 
Vokes & Vokes, 1983: 60, pl. 22, fig. 12. 

Description: Shell (Figs. 257-280) to 20 mm 
long, ovate-conic to elongate-oval, solid to 
thin, shiny to dull, often whitish, commonly a 
uniform yellowish to dark brown, with irregu- 
lar axial markings or with as many as five 
transverse brown bands on body whorl. Um- 
bilical excavation present. Spire low to mod- 
erately high, whorls eight to 11, flat, spirally 
pitted or grooved; apex frequently eroded. 
Body whorl about 85% of total length, stri- 
ated, with one, usually two or more incised 
striae on round shoulder. Aperture subaxial, 
about 90% body whorl length, narrow, with 
base moderately broadening; inner lip with 
small, oblique columellar tooth and two pari- 
etal teeth, the posterior strongest, perpen- 
dicular to columellar axis, anterior one 
minute, often absent; additional parietal den- 
ticles sometimes present; outer lip sharp, in- 
ternal lamellae uneven, white, as many as 17, 
not reaching edge and only three or four ex- 



264 



MARTINS 




FIGS. 257-276. 



WESTERN ATLANTIC ELLOBIIDAE 



265 




FIGS. 277-280. Melampus (M.) bidentatus, lateral and top views of spire and protoconch. (277) Hudson, 
Florida. (278) Jekyll Island, Georgia. (279) Long Key, Florida. (280) South Mastic Pt., Andros Island, Baha- 
mas. Scale, Fig. 279, 500 цт; all others, 1 mm. 



tend inward. Resorption of inner whorls ex- 
tensive, remaining internal partition less than 
half a turn (Fig. 267). Protoconch smooth, 
translucent, brownish (Figs. 277-280). 

Radula (Figs. 281-285) with formula [26 + 
(1 + 17) + 1 +(17 + 1) + 26] X 100. Radular 
morphology the same as that of Melampus 
(M.) coffeus. 

Animal as in Melampus (M.) coffeus. 



Stomach (Fig. 286) as in subfamily. 

Reproductive system basically as de- 
scribed under Melampus s.l.; posterior vas 
deferens about 70% of vagina length (Fig. 
287). 

Nervous system (Fig. 288) with left parietal 
ganglion one-fourth size of right one; visceral 
ganglion slightly larger than right parietal 
ganglion. Length of cerebral commissure 



FIGS. 257-276. Melampus (M.) bidentatus Say. (257) Neotype (USNM 859014), from Smith collection, St. 
John's River, Florida, si 9.2 mm. (258) Specimen figured by Binney (1865:10, fig. 11) (USNM 39818), si 14.8 
mm. (259) M. bidentatus var. lineatus Say, neotype (USNM 859013), Bivalve, New Jersey, si 8.1 mm. (260) 
Specimen figured by Binney (1865:10, fig. 12) (USNM 39818), si 12.6 mm. (261) Cedar Island, North 
Carolina, si 18.2 mm. (262) M. coffeus var. bisfiopi Davis, lectotype (ANSP 86925), South Shore, Bermuda, 
si 12.1 mm. (263) M. coffeus var. verticalis Davis, lectotype (ANSP 86927), South Shore, Bermuda, si 11.2 
mm. (264) M. coffeus var. alternatus Davis, lectotype (ANSP 86926), South Shore, Bermuda, si 11.6 mm. 
(265) Specimen figured by Binney (1859, pi. 75, fig. 30) as "Melampus floridanus Shuttleworth" (USNM 
39835), si 6.8 mm. (266) Crawl Key, Florida, si 2.15 mm. (267) Knight Key, Florida, si 14.8 mm. (268) Belize 
(USNM 426007a), si 12.0 mm. (269) Tampico, Mexico (USNM 219997a), si 8.8 mm. (270) Myrtle Grove, 
Louisiana (USNM 628753), si 15.0 mm. (271) Long Key, Florida (USNM 193363), si 18.8 mm. (272) Narrow 
River, Wakefield, Rhode Island, si 10.1 mm. (273) Narrow River, Wakefield, Rhode Island, si 12.6 mm. (274) 
Narrow River, Wakefield, Rhode Island, si 9.3 mm. (275) Narrow River, Wakefield, Rhode Island, si 10.7 mm. 
(276) Narrow River, Wakefield, Rhode Island, si 10.0 mm. 



266 



MARTINS 




FIGS. 281-284. Melampus (M.) bidentatus, radular teeth. (281) Narrow River, Rhode Island, sl 11.1 mm. 
(282, 283) Hungry Bay, Bermuda, s! 14.4 mm. (284) Skidaway Island, Georgia, sl 2.3 mm. Scale, Fig. 284, 
50 |im; all others, 100 цт. 



equals width of one cerebral ganglion; left 
pleuroparietal connective twice length of 
right pleuroparietal; left parietovisceral con- 
nective about half the length of right parieto- 
visceral. Internal palliai nerve crosses pneu- 
mostomal nerve to right, anastomoses with 
branch of medial palliai nerve, follows floor of 
pneumostome toward aperture and turns up 
to roof of mantle cavity, just to left of upper 
pneumostomal gland; pneumostomal nerve 
branches to mantle skirt, runs to pneumo- 
stomal aperture, sending branches along the 
way to mucous gland of mantle skirt, splitting 
to innervate lips of pneumostome. 



Remarks: Melampus (M.) bidentatus Say is 
more variable than any other Western Atlan- 
tic ellobiid. The shape of the shell (Figs. 257- 
276) varies from almost globose to moder- 
ately high spired and oval-elongate. The 
thickness of the shell shows a geographic 
gradient, increasing toward the warmer parts 
of the range; Auricula cornea from New York, 
described by Deshayes (1830), exemplifies 



the much thinner-shelled northern variety of 
Melampus (M.) bidentatus. The intergrading 
color pattern ranges from monochromic to 
axially striped to discretely banded, the latter 
pattern being common among juveniles. In 
some populations the size of some individu- 
als reaches that of some gerontic Melampus 
(M.) coffeus. The latter consistently has an 
accentuated conic shape as opposed to the 
slender profile of comparably-sized Melam- 
pus (M.) bidentatus. The number of riblets on 
the outer lip also shows geographical grada- 
tion with a tendency toward higher counts in 
the warmer parts of the range. These riblets 
are of unequal size and only four or fewer 
large ones penetrate deep into the aperture. 
As noted in the synonymy above, Melam- 
pus lineatus and Melampus obliquus, pro- 
posed by Say (1822: 246, 377, respectively), 
are here considered to be Melampus (M.) bi- 
dentatus. The name Melampus bidentatus 
was applied to the thin, monochromic east 
Florida specimens, Melampus lineatus to the 
smaller, banded variety of Melampus (M.) bi- 
dentatus from Maryland and New Jersey and 



WESTERN ATLANTIC ELLOBIIDAE 
С 1L 2L 12L Т 1М 2М 



267 




А 7М 8М 13М14М18М 19М20М 




С IL 17L Т 1М 




FIG. 285. Melampus (M.) bidentatus, radula. A, 
Woodville, North Carolina; В, Hudson, Florida. 
Scale 10 цт. 

Melampus obliquus to the rather thick form 
with a very oblique columellar tooth from 
South Carolina. 

Binney (1859: 159), who had access to the 
type material of Melampus bidentatus and 
Melampus lineatus, noted the variability of 
the species and wrote about the latter name, 
"I have met with none sufficiently marked to 
form a variety, much less a distinct species." 
Nevertheless, the name Melampus lineatus 
has been used to designate a subspecies or, 
erroneously, to substitute for Melampus (M.) 
bidentatus Say (Dall, 1885). The reasons for 
the use of Melampus lineatus resided in the 
misplacement of Auriculinella (Leucophytia) 




FIG. 286. Melampus (M.) bidentatus, 
North Carolina. Scale 1 mm. 



stomach, 



bidentata (Montagu, 1801) in the genus 
Melampus, which would have constituted a 
case of secondary homonymy. Dall's confu- 
sion arose from Binney's contention (1865) 
that the animal of Myosotella myosotis from 
America was apparently similar to Melampus 
(M.) bidentatus Say, and that it did not agree 
with the illustration oi Alexia given by H. & A. 
Adams (1855b, pi. 82, fig. 5). Binney did not 
say in what way they differed, however. Be- 
sides the color, the main difference between 
the animal of Myosotella myosotis (Drapar- 
naud) and that of Auriculinella (L) bidentata 
(Montagu, 1801) is that the foot of the latter 
species is transversely divided (Morton, 
1955b). Because Melampus has this same 
characteristic, Dall probably assumed that 
the Alexia myosotis referred to by Binney, like 
Melampus, would have a transversely di- 
vided foot. The shells of Myosotella myosotis 
and oí Auriculinella (L.) bidentata can be con- 
fused easily and Dall's (1885: pi. 18, fig. 13) 
illustration of Melampus (Leuconia) bidentata 
(Montagu) is a facsimile of Binney's (1865: 4, 
fig. 4) representation of Alexia myosotis. 

Say's last name, Melampus obliquus, was 
applied to a form similar to Melampus (D.) 
monile (Bruguière, 1789). Say (1822: 377) 
added that in the collection of the Academy 
of Natural Sciences of Philadelphia there 
were specimens from the West Indies which 
conformed with his description of Melampus 
obliquus. Binney (1859: 167), who had seen 



268 



MARTINS 




FIG. 287. Melampus (M.) bidentatus, reproductive system. A, Narrow River, Rhode Island; B, Cedar Island, 
North Carolina; C, New Smyrna, Florida; D, Hungry Bay, Bermuda. Scale 1 mm. 



specimens belonging to the first two of Say's 
names, noted, "It is not known what shell 
Say had in view when the above description 
was written. No authentic specimen was pre- 
served, and no author has seen any shell 
from that locality answering to the characters 
laid down." In 1865 Binney relegated Say's 
Melampus obliquas to his "Spurious species 
of Melampus.'' On Cedar Island, North Caro- 
lina, however, I found specimens of Melam- 
pus (M.) bidentatus that fit Say's description 
of Melampus obliquus (Fig. 261). Melampus 
obliquus Say must, then, be treated as a jun- 
ior synonym of Melampus (M.) bidentatus 
Say. 

Pfeiffer introduced several species that 
should be related to Melampus (M.) bidenta- 
tus. In his comments on Melampus gundlachi 
from Cayo Blanco, Cuba, Pfeiffer (1853b) 
noted that their juveniles were much more 
brightly colored than those of Melampus (M.) 
coffeus and he did not mention incised 
grooves. The elliptic-ovate shape of the shell. 



however, indicates to me that Pfeiffer's name 
can be treated as a synonym of Melampus 
(M.) bidentatus Say. 

Another of Pfeiffer's (1854a) introductions, 
Melampus redfieldi from Bermuda, was dis- 
tinguished from Melampus (M.) coffeus by 
the presence of very compressed riblets in 
the outer lip. Because it occurs in the latter 
species (personal observation), this condition 
is not a useful character. The fact that Pfeiffer 
referred to the striations on the shell sug- 
gests that he was actually describing a spec- 
imen of Melampus (M.) bidentatus. 

Pfeiffer (1854b, 1856a) erroneously identi- 
fied a variety of Melampus (M.) bidentatus 
Say with Melampus borealis (Conrad) [= My- 
osotella myosotis (Draparnaud)]. Neither 
Pfeiffer's description nor the locality given 
(Georgia) agrees with those of Conrad (1 832). 
Pfeiffer (1876: 316) later explained that he 
was referring to a museum label in the Cum- 
ing collection, rather than to Conrad (1832). 

In 1841 Mittré described Auricula jaumei 



WESTERN ATIJ\NTIC ELLOBIIDAE 



269 




FIG. 287. 



from Hampton, Virginia. It was said to differ 
from Deshayes' Auricula cornea in having the 
inside of the outer lip consistently ribbed. 
Melampus (M.) bidentatus is highly variable in 
this respect (Holle & Dineen, 1959) and this 
character is therefore unreliable fortaxonomy. 
Auricula jaumei is conspecific with Melampus 
(M.) bidentatus. 

Melvill (1881) mentioned Melampus spiralis 
Pfeiffer from Cedar Keys, on the western 
coast of Florida. Pfeiffer (1856a), however, in 
his observations on Melampus spiralis, noted 
that this species was made known to him by 



Cuming as Melampus pallescentis Sowerby, 
1839. Because Sowerby provided an incom- 
plete description of the latter taxon, Pfeiffer, 
based on Sowerby's figure (1 839a in Beechy: 
pi. 38, fig. 28), thought that Melampus pall- 
escentis Sowerby should be referred to 
Melampus luteus Quoy & Gaimard, 1832, 
from the Philippines. It appears, then, that the 
Melampus spiralis of Pfeiffer was not based 
on West Indian material. Melvill's citation 
(1881) of "Melampus spiralis Pfeiffer" should 
be treated as a misidentification of Melampus 
(M.) bidentatus. 



270 



MARTINS 




spc pg plprc pipe 




vg prvc prg Plg PC epic eg 



cbc be 



FIG. 288. Melampus (M.) bidentatus, central ner- 
vous system. A, Narrow River, Rhode Island; B, 
New/ Smyrna, Florida. Scale 1 mm. 



Morrison (1951b) recognized several sub- 
species of Melampus (M.) bidentatus: M. b. 
corneus from Prince Edward Island, Canada, 
to Staten Island, New York; M. b. lineatus 
from New Jersey to North Carolina; M. b. bi- 
dentatus from South Carolina to Florida, 
Texas and the West Indies; and M. b. redfieldi 
from Bermuda. The latter supposed subspe- 
cies also lives in Florida (Pfeiffer, 1876, with a 
question mark; personal observation) and 
shows as much variation as the other forms 
of Melampus (M.) bidentatus. Shell thickness 
and color seem to be linked to temperature, 
the thinner and paler forms being typical of 
colder regions. This link would account for 
the similarities between shells from Bermuda 
and those from Florida (see the remarks un- 
der Myosotella myosotis). Holle & Dineen 
(1959) reported the continuous variation in 
shell characters along the range of the spe- 
cies, thus rendering Morrison's treating the 
morphs as subspecies unjustifiable. 

Morrison (1951b, 1964) placed Melampus 
(M.) bidentatus in the subgenus Micromel- 
ampus Möllendorff, 1898, which had been 
erected, according to Zilch (1959), to include 
the small Melampus. Only anatomical study 



of the type species, Melampus nucleolus 
Martens, 1865, from Amboina, will allow an 
objective decision concerning the taxonomic 
status of this subgenus. In any case, the ob- 
served wide range of size in Melampus (M.) 
bidentatus does not justify its inclusion in the 
subgenus Micromelampus and my anatomi- 
cal study strongly favors its inclusion in 
Melampus s.s. 

It appears that Say's type material, to 
which Binney referred (1859), is not in the 
Academy of Natural Sciences of Philadelphia 
and was presumed lost (Holle & Dineen, 
1959; Baker, 1964). Because of documented 
confusion between Melampus (M.) bidenta- 
tus and Melampus (M.) coffeus, neotypes 
that conform to original descriptions and ac- 
cepted usage are herein designated for 
Melampus bidentatus and Melampus linea- 
tus. Inspection of material from South Caro- 
lina present in the collections of the various 
museums did not provide any specimens 
that could be identified with Say's Melampus 
obliquus. As noted above, I found on Cedar 
Island, North Carolina, a colony of Melampus 
(M.) bidentatus that agree with Say's descrip- 
tion of Melampus obliquus. Without ade- 
quate material from the type locality. South 
Carolina, and with the disuse into which 
Say's name has fallen, it is inappropriate and 
unnecessary to designate a neotype for 
Melampus obliquus. 

Habitat: The salt-marsh snail, Melampus (M.) 
bidentatus, is very common in the high-tide 
fringe of salt marshes and mangroves. Its 
habits have been studied only in the New En- 
gland area, in which this mollusk lacks con- 
generic competitors. When Say described 
this species (1822) he noted its abundance 
and he considered it an important item in the 
diet of marsh birds. 

Although dependent upon the rhythm of 
the tides, the salt-marsh snails are more ac- 
tive during the low tides at twilight. Their diet 
includes diatoms and detritus of vegetal and 
animal origin (Hausman, 1936; Thompson, 
1984). The animals gather to spend the win- 
ter in partial hibernation (Grandy, 1972). 

Apley (1970) and Russell-Hunter et al. 
(1972) provided detailed studies of the early 
life-history of this species. The snails become 
sexually mature at a shell length of 5 to 6 mm 
and have a life span of three to four years. 
Copulation and hatching of veliger larvae are 
closely synchronized with spring tides. Ge- 
latinous masses of eggs are laid within one 



WESTERN ATLANTIC ELLOBIIDAE 



271 




FIG. 289. Melampus (M.) bidentatus, geographic 
distribution. 



day after copulation. About 13 days later 
free-swimming veligers hatch and spend 
about six weeks in the plankton before set- 
tling. 

In the mangroves Melampus (M.) bidenta- 
tus commonly lives under fallen leaves and 
debris at the high-tide fringe, and is abundant 
on the margins of sheltered inland lagoons. In 
this habitat it coexists with Melampus (M.) 
coffeus. 

Range: New Brunswick, Canada, to the Flor- 
ida Keys, the Gulf coast of the United States 
south to Belize; Bermuda; Bahamas, Cuba, 
Jamaica, Hispaniola, Tórtola (Fig. 289). The 
Tórtola record is suspect and has not been 
confirmed by recent collections. 

Specimens Examined: NEW BRUNSWICK: 
Buctouche Bay (MCZ 200471). PRINCE ED- 
WARD ISLAND (MCZ 34048): Mount Stuart 
(ANSP 106545); Bunbury (ANSP 106678, 
106938). NOVA SCOTIA: Windsor (ANSP 
326060); West Peswick, Halifax (MCZ 
297898). MAINE: Newmeadows River (MCZ 
104992); Middle Bay (MCZ 294188); Cape 
Elizabeth (USNM 1 29331 , 1 90466); Biddeford 
(ANSP 22370, 77421, 242121; MCZ 34049, 
34810); USNM 492528). NEW HAMPSHIRE: 



Jackson's Landing, Durham (MCZ 193855); 
Sagamore Creek (MCZ 275395). MASSA- 
CHUSETTS (MCZ 201644): Ipswich (MCZ 
147833); Gloucester (ANSP 102400; MCZ 
201639; USNM 159104); Bass Rocks, 
Gloucester (USNM 408730); Goodharbor 
Beach, East Gloucester (MCZ 199906); 
Manchester (USNM 398130); Danvers (MCZ 
3963, 34052, 61 508, 1 331 95; USNM 504484); 
Salem (MCZ 201 633, 201636; USNM 73424); 
Lynn (MCZ 34053; USNM 224905); Revere 
(ANSP 89557); Revere Beach (MCZ 147714, 
199909); Magazine, Cambhdgeporl (MCZ 
141058; USNM 590055, 600303); Charles 
River, Boston (ANSP 56837); Boston Harbor 
(MCZ 141060); Neponset River, Milton (MCZ 
142330); East Milton (MCZ 55146); Cohasset, 
Norlh Scituate (MCZ 139271); Duxbury (MCZ 
14884, 163165, 201638; USNM 492523, 
492525, 492535); Gurnet Lights, Plymouth 
(MCZ 199905); Barnstable (ANSP 44599, 
56840; USNM 34404, 159105, 487652); 
Sandy Neck (MCZ 182392); Truro (USNM 
603101); Playground Beach, Hyannis (ANSP 
176264); Wellfleet (R.B.); Provincetown 
(ANSP 1 34441 ; MCZ 1 4771 5, 1 9991 1 ; USNM 
159108, 307158, 341102, 341104, 492532, 
492533, 492536); Buzzard's Bay (MCZ 
199913); Eastham (MCZ 199907, 201632); 
Pleasant Bay (MCZ 80561); Chatham (MCZ 
34054); Eel Pond, South Chatham (MCZ 
18812); South Dennis (MCZ 14547; USNM 
492526); Grand Cove, South Dennis (MCZ 
1 4548); Point Gammon, West Yarmouth (MCZ 
112213); Lewis Bay (MCZ 200027); Nobska 
Point (MCZ 140811); Briar Neck (MCZ 
199904); Vineyard Sound (USNM 159107); 
Nantucket (MCZ 34047); SE of Coskatee, 
Nantucket (MCZ 167949); South Beach, Nan- 
tucket Harbor (MCZ 167450); Popponesset 
Beach (MCZ 1 82391 ); Waquoit (ANSP 46678); 
Naushon Island (ANSP 163469; USNM 
159110); Great Pond, Falmouth (USNM 
660507); Woods Hole (MCZ 34051, 199908; 
USNM 159106); Bathing Beach, Woods Hole 
(USNM 340981, 340983, 340984; Little Sip- 
pewisset Marsh, Falmouth (MCZ 294115; 
A.M.); West Falmouth (ANSP 76171); Ware- 
ham (MCZ 34050, 1 9991 0); Piney Point, Mar- 
ion (MCZ 178105); New Bedford (ANSP 
56846; MCZ 201635). RHODE ISLAND: New- 
port (ANSP 56838; USNM 39814, 159109); 
Nayatt (MCZ 71 268, 1 9991 4; Jamestown, Co- 
nanicut Island (A.M.); Seekonk River (ANSP 
243912; MCZ 199912); Pawtuxet (MCZ 
68940); Buttonwoods (MCZ 199915; USNM 
492530); Apponaug (MCZ 151930; USNM 



272 



MARTINS 



568388); Wakefield, Pettaquamscutt River 
[Narrow River] (A.M.); Westerly (MCZ 14550; 
USNM 492541, 590089). CONNECTICUT; 
Stonington (ANSP 91947; MCZ 3965, 56902, 
133196; USNM 858073; A.M.); Long Beach 
(MCZ 231486); Oxecoset Brook (A.M.); Guil- 
ford (USNM 478030, 568440); Pine Orchard 
(MCZ 166061, 201630); Branford (MCZ 
34055, 34925, 199916); New Haven (MCZ 
291293; USNM 404295); Lighthouse, New 
Haven (USNM 380818); Greenwich (ANSP 
154660). NEW YORK: Harlem River (MCZ 
156659, 167630; USNM 492538); Long Island 
(MCZ 201637, 230929; USNM 307157 
492527, 492542); Greenport (MCZ 161271 
USNM 407784); Sand's Point (ANSP 1 45457) 
Sea Cliff (ANSP 43785); Oyster Bay (USNM 
307154); Cold Spring (USNM 504486); Towo 
Point (USNM 694036); Orient (ANSP 133707, 
218373; MCZ 124210); Shelter Island (ANSP 
362811); East Patachogue (MCZ 288109); 
Freeport (MCZ 248224); Coney Island (ANSP 
362808); Far Rockaway (MCZ 54518, 
139569); Sheepshead (MCZ 156658); Staten 
Island (ANSP 132043; MCZ 78422, 201631; 
USNM 59725, 307159, 492500b). NEW JER- 
SEY: Raritan Bay (USNM 608377); Union 
Beach, Raritan Bay (USNM 606609); E of Nan- 
tuxant Point, Newport (ANSP 162143); Point 
Pleasant (ANSP 65200); Harvey Cedars, Long 
Beach Island (ANSP 106527); Beach Haven 
(ANSP 155518); Shrewsbury River (ANSP 
99006); Brigantine Island (ANSP 195015, 
328333; USNM 611523); Atlantic City (ANSP 
56843; MCZ 188902; USNM 492524); Vent- 
nor (ANSP 99155); Margate City (ANSP 
451 92); Great Egg Harbor Bay (ANSP 326220; 
A.M.); Avalen (ANSP 354825); Wildwood 
Beach (ANSP 78982, 194600); Cape May 
(ANSP 45098, 65201, 106229. 110131, 
117532; USNM 119503, 124603, 406309, 
504479); Cape May Harbor (ANSP 182641); 
Carson's Inlet (ANSP 133907); Bivalve (ANSP 
113465; A.M.); Dividing Creek (A.M.); Fortes- 
cue (ANSP 113466). DELAWARE: Woodland 
Beach (USNM 522267); Rockhall (ANSP 
112612); S of Fort Miles (USNM 621420); In- 
dian River Inlet (MCZ 1 98052); N end of Cedar 
Neck, S side of Indian River Bay (USNM 
621418, 621419); Mouth of Cedar Creek 
(USNM 406310); Assawoman Wildlife Area 
(ANSP 302221). MARYLAND: Mayo Beach 
(USNM 522288); Galesville (USNM 595602); 
Chesapeake Beach (USNM 191 595, 473893); 
Parkers Creek (USNM 521920, 536709); near 
Triton Beach (758314); Piney Island (USNM 
667267); Patuxent River (ANSP 396602; MCZ 



139263); Carrolls Bank, mouth of Patuxent 
River (USNM 363927); Broome Island (USNM 
473465); N of Solomons Island (USNM 
600765); Solomons Island (USNM 424040); 
Millstone Landing (USNM 512876); Benedict 
(USNM 473456); St. Marys River (USNM 
379539); Smiths Creek (USNM 518853); 
Cobb Island (USNM 499519, 522921); Island 
Creek (USNM 252064); Hope House, N of 
Easton (USNM 602855); Huggins Point, S of 
Leonard Town (MCZ 216712); Town Point 
(ANSP 132462; MCZ 46420, 52344); Church 
Creek, Cambridge (MCZ 200468); Parsons 
Creek (MCZ 211150); Bishops Head (MCZ 
139264); Ocean City, Sinepuxent Bay (USNM 
601 744, 601 747); E of Dames Ouarter (USNM 
618922); SE of Chance Island (USNM 
473331); Deal Island (USNM 468283); Cris- 
field (USNM 595598); near Snow Hill, Chin- 
coteague Bay (USNM 605563); West Bay, 
Chincoteague Bay (USNM 591783). VIR- 
GINIA: Chincoteague Island (MCZ 199443; 
USNM 530826, 533596); Oyster (USNM 
407459); Magotha (ANSP 275980; USNM 
422297); Smiths Island (USNM 153352, 
225965, 422294, 422295); Dameron Marsh, 
Balls Creek and Ingram Bay (ANSP 305137); 
Fisherman Island (USNM 422293); Brighton 
(USNM 171118); Assateague Island (ANSP 
352439; USNM 809536); Toms Cove, As- 
sateague Island (USNM 209268); Watts Bay 
(USNM 701629); Fairport (USNM 103258); 
Potomac Beach (USNM 473900); Wicomico 
Church (USNM 269147); Bretton Bay (USNM 
628900); Greenvale Creek near Rappahan- 
nock (MCZ 214466, 291314); Sweetheart Is- 
land (USNM 269077); Fleeton (USNM 
308939); Severn River (USNM 679373); Chis- 
man Creek (USNM 603690); Poropotank, 
York River (USNM 679375); Goodwin Island 
(USNM 679374); Yorktown (USNM 474077); 
Norfolk (MCZ 46542; USNM 407588, 504483, 
539235, 667497); Granby and Lakewood 
bridge, Norfolk (ANSP 219145; MCZ 221231; 
USNM 653497); Boissevain Avenue, Norfolk 
(ANSP 263386; MCZ 1 86692); Lamberts Point 
(ANSP 263388); Elizabeth River (MCZ 
186696); Lafayette Park, on bank of Lafayette 
River (MCZ 186691). NORTH CAROLINA: 
Bodie Island (MCZ 105478); Pee Island 
(USNM 488826); Hatteras Island (USNM 
637152); Cedar Island (A.M.); North River, 
Woodville (A.M.); Williston (A.M.); Oyster 
Creek (A.M.); Beaufort (ANSP 56839, 145683; 
USNM 380566, 382982, 433203. 523610, 
523620); Mullet Pond, Beaufort (USNM 
380565); Brackish Pond (MCZ 141059); North 



WESTERN ATLANTIC ELLOBIIDAE 



273 



River (ANSP 179830; MCZ 81930); Newport 
River (A.M.); Whghtsville (USNM 492540); 
Southport (ANSP 113647, 227028; MCZ 
176143); Smith Island, Cape Fear (ANSP 
95602); Cape Fear River (MCZ 175210). 
SOUTH CAROLINA: Pawleys Island (MCZ 
201642); Bull Island (USNM 543341); Sulli- 
vans Island (USNM 492537); Charleston 
(ANSP 56884; USNM 26571, 26574, 39823, 
307156); Folly Beach (ANSP 300432); Edisto 
Island (USNM 474096); Edisto Beach (ANSP 
180786); Yemassee (USNM 492539; A.M.); 
Lobeco (A.M.); Pocataligo (USNM 6031 06); N 
of McCIellanville (USNM 758249). GEORGIA 
(ANSP 56835): Skidaway Island (A.M.); Cox- 
boro Island (USNM 622491); Savannah (MCZ 
200467; USNM 610311, 665761, 665762); 
Jones Island, Savannah River (ANSP 1 64988); 
Crescent (A.M.); Valona (A.M.); Fort King 
George, Darien (USNM 707263); Sea Island 
(ANSP 56847); Saint Simons Island (ANSP 
123529); Brunswick (ANSP 183414; MCZ 
186697; USNM 425961; A.M.); Jekyll Island 
(A.M.). FLORIDA: Fernandina (MCZ 201208); 
St. John's River (USNM 307155); Mayport 
(ANSP 56844, 76095); Jacksonville (ANSP 
56841; USNM 39815); St. Augustine (ANSP 
45077, 66965, 140731; MCZ 186695; USNM 
36014, 39825a, 492529); Fort Marion, St. Au- 
gustine (ANSP 9523); Matanzas (USNM 
672437); Indian River (MCZ 186699, 291315 
USNM 758221); Ormond Beach (MCZ 82493) 
New Smyrna Beach (MCZ 291 026; A.M.); Oak 
Hill (ANSP 22362; MCZ 201640; USNM 
87624); Titusville (MCZ 143992); Banana 
River (MCZ 201643); Grant (MCZ 105475); 
Lake Worth (ANSP 69851; MCZ 291287; 
USNM 253538); Fort Dallas (USNM 39817, 
1 1 9502); Haulover Canal, head of Indian River 
(ANSP 62720); Miami (ANSP 77506, 82844, 
1 45885); Biscayne Bay (MCZ 291 305); Sands 
Key (MCZ 291309); Virginia Key, Biscayne 
Bay (ANSP 189570); Coconut Grove (MCZ 
291299, 291300; USNM 603111); Waveland 
(USNM 103495, 123532); Madero Bay (MCZ 
291289); Soldier Key (MCZ 174457); Middle 
Key, Barnes Sound (USNM 405985); McGinty 
Key (ANSP 189572; MCZ 103303); Pumpkin 
Key (USNM 355115); Tavernier (MCZ 
294246); Key Largo (ANSP 294318; MCZ 
291281, 291302, 291313, 294228; USNM 
603119); Tavernier Creek (USNM 667401; 
A.M.); Tavernier Key (USNM 492549, 
492552); Snake Creek (MCZ 294234); Plan- 
tation Key (MCZ, 294230, 294231; A.M.); 
Windley Key (USNM 603104); Indian Key 
(USNM 26423, 27917, 462894a); Indian Key 



Fill (A.M.); Lignumvitae Key (ANSP 156327, 
189571); Lower Matecumbe Key (MCZ 
291294; USNM 492553); Long Key (ANSP 
76700; MCZ 291 296, 291 031 ; USNM 1 93363, 
492578; A.M.); Grassy Key (MCZ 291288; 
A.M.); Crawl Key (MCZ 174458, 291032, 
291033, 294235; A.M.); Marathon, Key Vaca 
(ANSP 189584); Knight Key (A.M.); Bahia 
Honda Key (ANSP 104095; USNM 269777a, 
27031 0); West Summerland Key (A.M.); New- 
found Harbor (USNM 272688a); Little Pine 
Key (USNM 681642); Big Pine Key (ANSP 
104092, 104093; MCZ 291029, 291034, 
294237, 294243; USNM 597453; A.M.); Big 
Torch Key (ANSP 104096; A.M.); Howe Key 
(USNM 681641); Ramrod Key (MCZ 291028, 
291045, 294232, 294233); Sugarloaf Key 
(ANSP 104094); Big Coppit Key (USNM 
603102); Boca Chica Key (ANSP 104091, 
152501; USNM 270326, 511180); Stock Is- 
land (ANSP 149993; MCZ 59993; USNM 
270269); Key West (ANSP 294309; MCZ 
9947; USNM 27730, 529557, 596787, 
667405, 670450); Shark Key (USNM 696979, 
711532); Boca Grande Key (USNM 270262); 
Flamingo Key (ANSP 294312; MCZ 291038, 
294236, 294244); Cape Sable (MCZ 291035); 
Lossman River (ANSP 132369); Everglades 
City (USNM 683928); Marco Island (MCZ 
294249); Little Marco (USNM 51 1210); Naples 
(ANSP 1 89568; MCZ 291 31 6); Sanibel (ANSP 
170640; MCZ 13278, 13279, 294239, 
294248); Pineaire, Pine Island (MCZ 291030); 
Bokeelia (MCZ 294245; A.M.); Matlacha 
Key (MCZ 291311); Starvation Key (ANSP 
294320); Captiva Island (MCZ 294250); Punta 
Gorda (USNM 492577); between Fort Myers 
and Punta Gorda (USNM 531133); Charlotte 
Harbor Bay (USNM 407410); Boca Grande, 
Gasparilla Island (ANSP 142272); Little Gas- 
parilla Island (ANSP 189592); Sarasota 
(USNM 159254, 487213, 487314); 5 km N of 
Sarasota (ANSP 195406); Long Boat Key 
(MCZ 294252); between Palma Sola and Cor- 
tez (MCZ 291037); Anna Maria Key (MCZ 
291027); Palmetto (A.M.); Manatee River 
(MCZ 3969; USNM 61052); Small Island, 
mouth of Manatee River (MCZ 291282); Big 
Bend Road [Rt. 672] (A.M.); Tampa (ANSP 
56836, 294317, 362807; MCZ 201649, 
291284, 294238; USNM 36061, 37609, 
193361, 196349, 492574, 504487); Young 
Lagoon, Tampa (USNM 37610); Hillsborough 
River (USNM 100693); Palm River (MCZ 
201647); Mullet Key (A.M.); Shell Key (USNM 
466206a, 466288); S of Pass-a-grille (MCZ 
201685, 291285, 294241); Pass-a-grille 



274 



MARTINS 



(ANSP 294321); Pinellas Point (MCZ 294190; 
USNM 194730); St. Petersburg (ANSP 
132371, 132372, 132373, 132374; USNM 
341721, 466194); Bird Key (ANSP 43568); 
Gulfport (MCZ 294242); Boca Ciega Bay 
(ANSP 189574; USNM 341722); Clearwater 
(ANSP 189569, 294319, 294322; MCZ 
294247; USNM 611786a); Anclote River 
(A.M.); Hudson (A.M.); Aripeka (ANSP 73902, 
151138, 151257); Little Blind Creek (ANSP 
149525); Cedar Key (ANSP 56842, 194040, 
194227, 362810; MCZ 199316, 201653, 
201656, 291279; USNM 36012, 36013, 
61700); Suwannee (ANSP 88138; MCZ 
1 9931 5); Jena (USNM 484844); Adams Beach 
(MCZ 186701); St. Marks (ANSP 56814, 
56816); Panacea (MCZ 91696; USNM 
706611); St. Andrews Bay (ANSP 83641; 
USNM 667402, 667403, 667404); Anderson's 
Bayou, St. Andrews Bay (ANSP 83653); 
Ochlockonee (MCZ 1 9931 7); Port St. Joe Bay 
(MCZ 29130, 291297); Panama City (MCZ 
235949). AIJ\BAMA: Cedar Point (MCZ 
1 86702); Heron Bay (ANSP 31 571 0); Dauphin 
Island (USNM 701860); Coden Beach (USNM 
422364); St. Anthony Bay (ANSP 365474). 
MISSISSIPPI: Boat Harbor at Ocean Springs 
(MCZ uncatalogued). LOUISIANA: Chan- 
deleur Islands (USNM 189168); Grand Isle 
(MCZ 186700; USNM 603100); Cherniere-au- 
Tigre (ANSP 145106); Fort Pike, Orleans Par- 
ish (MCZ 251101); Houma (USNM 653314); 
Grand Lake, Calcasieu (USNM 160814, 
46701 5); Myrtle Grove (USNM 628753); Cam- 
eron (USNM 177952). TEXAS: Galveston 
(ANSP 69414, 71522, 73692); East Lagoon, 
Galveston (MCZ 217872); Seabrook (ANSP 
105895); Clearlake (MCZ 217874); Quitano 
Beach (MCZ 227841; USNM 600177); Free- 
port (ANSP 254824); Matagorda (USNM 
1 25534); La Vaca, La Vaca Bay (MCZ 223041 ; 
USNM 126755); Sand Point, Keller Bay 
(USNM 464802, 465269, 465278); Indianola 
(USNM 26425, 26572, 39832); Rockport 
(MCZ 217875); Carancahua Bay (USNM 
1 34435); Aransas Pass (ANSP 3221 51 ; USNM 
603108); Ransom Island (MCZ 200470); Ran- 
som Island, Redfish Bay (MCZ 198174); Port 
Aransas (ANSP 284785); Mustang Island 
(MCZ 217873); Corpus Christi (MCZ 294191 
USNM 603107); Port Isabel (ANSP 80044 
MCZ 193910; USNM 603109, 603110) 
Brownsville (ANSP 351204); Callo del Oro 
(USNM 473355). MEXICO: Tampico (USNM 
219997a); N end of Ascension Bay, Quintana 
Roo (USNM 735992, 735993, 736143); near 
Allen Point, Ascension Bay, Quintana Roo 



(USNM 736693). BELIZE: Belize (ANSP 
96583); Botanical Garden (USNM 426007a). 
BERMUDA (ANSP 56815, 56817, 56819, 
56823, 77905; MCZ 3972, 9949, 201106, 
201663, 201667, 201674, 201676, 291290, 
291303, 291307, 291312; USNM 6540, 
11420, 37605, 39805, 94432, 94433, 98152, 
173643, 173644, 173645, 173646, 173647, 
492582, 492584): Fairyland (ANSP 99053); 
Hamilton Island (MCZ 201105); Hungry Bay 
(ANSP 85712; MCZ 10381, 24248, 48123, 
291306; USNM 492578, 492583; A.M.); South 
Shore (ANSP 86925, 86926, 86927; MCZ 
53060, 53061, 53062; USNM 109557, 
109558, 109559); Ely's Harbour (A.M.). BA- 
HAMA ISLANDS (MCZ 54619): GRAND BA- 
HAMA ISLAND: Bootle Bay (ANSP 371880); 
North Hawksbill Creek (ANSP 370567); 
GREAT ABACO ISLAND: Witch Point (ANSP 
359151; USNM 492565, 492580b); Mastic 
Point Creek (USNM 618607); Angelfish Point 
(MCZ 116711); BIMINI: Mangrove Creek 
(ANSP 325614); Mosquito Point (ANSP 
326148); BERRY ISLANDS (MCZ 294251); 
ANDROS ISLAND: Morgan's Bluff (A.M.); 
South Mastic Point (A.M.); Mangrove Cay 
(ANSP 189587; USNM 269477, 269855, 
269968a, 27021 4d, 270216); Under Key 
(USNM 269360, 270483); NEW PROVIDENCE 
ISLAND: Nassau (USNM 160766); Dick's 
Point (MCZ 291280); South Beach, Fox Hill 
(MCZ 294240); Bonefish Pond (USNM 
618645; A.M.); Millars Sound (A.M.); Millars 
Road (A.M.); ROYAL ISLAND (USNM 
468115); ELEUTHERA ISLAND: Rock Sound 
(MCZ 135932); CAT ISLAND: Russell Creek 
(ANSP 294330; MCZ 291278, 294229) 
Arthurstown (MCZ 291295); EXUMA CAYS 
Hog Cay (ANSP 285755); LONG ISLAND 
Brett's Hill (MCZ 113332, 291283, 291286) 
Clarencetown (ANSP 173261); Glenton's 
(ANSP 1 89573; MCZ 291 291 ); Pinder's (MCZ 
113330); Salt Pond, Clarencetown (USNM 
595950); AKLINS ISLAND: Pinnacle Point 
(USNM 390856, 392237); Rooker Cay (USNM 
390674); CAY SAL BANK: CAY SAL (MCZ 
291331). TURK'S & CAICOS: TURK'S IS- 
LAND: (USNM 492474a). CUBA (ANSP 
56794, 56795, 56820, 189584): Bahia de 
Santa Rosa (USNM 492556a); Dimas (USNM 
492559); Cayo de las Cinco Léguas (ANSP 
294325); Cayo Perro, Cárdenas (ANSP 
189589); Mahanao (ANSP 294324); Cayo 
Maya, near Cayo Santa Mana (MCZ 294187); 
Cayo Juan Garcia (MCZ 291308); Isla de Co- 
bos (MCZ 294186); Cayo Romano (MCZ 
291309); Gibara (USNM 603097); Finca, Sa- 



WESTERN ATU\NTIC ELLOBIIDAE 



275 



banalmar (MCZ 294189); Punta de los Colo- 
rados, Bahia de Cienfuegos (MCZ 291292); 
Alto del Caracol, Caracoles, S of Pinar del Rio 
(MCZ 201675); Isla de Pinos (MCZ 48079; 
USNM 130028). JAMAICA (ANSP 56793); 
Green Island Harbor (USNM 440805a); Pali- 
sadoes (USNM 713079). HAITI; Gonave Is- 
land (USNM 492531a). DOMINICAN REPUB- 
LIC; Isla La Matica, Playa Boca Chica, E of 
Santo Domingo (R.B.). VIRGIN ISLANDS; ? 
TÓRTOLA (USNM 6485). 

Subgenus Detracia Gray, 1840 

Detracia Gray, 1840; 20. Type species by 
monotypy; Detracia bullaeoides (Mon- 
tagu, 1808) [unjustified emendation of 
bullaoides]. 

Tifata H. & A. Adams, 1855b; 245. Type spe- 
cies herein designated; Tralia (Tifata) 
globulus (Orbigny, 1837). 

Ensiphorus Conrad, 1862; 571. Type species 
by monotypy; Melampus (Ensiphorus) 
longidens Conrad, 1862 [Miocene]. 

Eusiphorus Conrad. Zilch, 1959; 65 [error for 
Ensiphorus; in synonymy]. 

Description: Shell globose to oval-oblong to 
fusiform; spire low to high, whorls ten to 13; 
aperture very narrow; columellar tooth ob- 
lique and stronger than parietal teeth; parti- 
tion of inner whorls occupying almost all of 
body whorl, parietal teeth continuing on wall 
of inner whorl as conspicuous lamellae. Ani- 
mal grayish blue to dirty white, sometimes 
mottled with dark brown spots. Conspicuous 
medial nodes on base of central radular 
tooth. Visceral mass separated from foot by a 
length equivalent to about one and one-half 
whorls; mantle organ forming conspicuous 
pouch; palliai gonoducts and cephalopedal 
reproductive organs elongate. 

Remarks: Detracia was created by Gray 
(1840) for the West Indian species Melampus 
bullaoides (Montagu) because it was said to 
have only the columellar tooth on the inner 
lip. Careful inspection of Melampus (D.) bul- 
laoides reveals a hidden parietal tooth mid- 
way on the inner lip and a long, vertical, cal- 
lous anterior parietal tooth. The most obvious 
diagnostic feature is the very strong, oblique 
columellar tooth. 

The genus Tifata was introduced by H. & A. 
Adams (1855b) as a subgenus of Tralia and 
was characterized by having two spiral, ele- 
vated, lamellar plates at the forepart of the 
inner lip. The genus Tralia had been intro- 



duced by Gray (1840) on account of the 
shape of the outer lip, but H. & A. Adams 
(1855b), followed by Binney (1865), used the 
incorrect anatomical feature, "foot posteri- 
orly acute," to separate this taxon from 
Melampus (Fischer & Crosse, 1880; Dall, 
1885). This led to the erroneous inclusion of 
Tifata within the genus Tralia. The pattern of 
dentition of the inner lip used by the Adams 
brothers to characterize Tifata is not con- 
spicuous in the first two originally included 
species, Tralia cingulata (Pfeiffer, 1840) [= 
Melampus (D.) bullaoides (Montagu, 1808)] 
and Tralia floridana (Pfeiffer, 1 856) [= Melam- 
pus (D.) floridanus]. In those species the first 
parietal tooth is usually a broad, longitudinal 
callosity, and the lamellar second parietal 
tooth is too far posterior in the aperture to be 
considered in the "forepart" of the inner lip. 
In the next species listed, Tralia globulus (Or- 
bigny, 1837) [= Melampus (D.) globulus], the 
longitudinal callosity is less pronounced, re- 
sembling more an oblique lamella (Keen, 
1971; fig. 2402). This agreement with the 
original description justifies my choice of Tra- 
lia globulus as type species of the subgenus 
Tifata; to clarify further the taxonomy, I 
hereby select a lectotype for this species 
(Fig. 320). Nevertheless, all species originally 
included in Tifata H. & A. Adams, including 
Tralia pulchella (Petit, 1843), should be 
placed in Detracia on the basis of the strong, 
oblique columellar fold. 

Morrison (1951b, 1964) considered 
Melampus (D.) monile (Bruguière, 1789) to 
belong to Pira H. & A. Adams, 1 855, which he 
elevated to generic rank. Pira was character- 
ized as having three teeth on the inner lip. 
The type species. Auricula kuesteri (Krauss 
MS) Küster, 1844 [= Melampus fasciatus (De- 
shayes, 1830)], was illustrated by Küster 
(1844; 34-35, pi. 4, figs. 10-13), who noted 
the conspicuous twisted columellar tooth. Its 
relative prominence is evident in his figure 13, 
which represents Küster's variety A of that 
species. Although a decision on the system- 
atic status of Pira is at present unwarranted 
owing to lack of anatomical data for compar- 
isons, Melampus monile (Bruguière) should 
be included in Detracia on the basis of shell 
and anatomical characters. 

Conrad (1862) introduced Ensiphorus for a 
Miocene species from Yorktown, Virginia, 
that was characterized by its elongate, 
slightly curved columellar tooth directed ob- 
liquely upwards, a characteristic of Melam- 
pus (D.) morhsoni. The type species, Ensi- 



276 



MARTINS 



phorus longidens, illustrated by Conrad 
(1866, pl. 4, fig. 12), resembles in its size and 
shape a small Melampus (D.) bullaoides or a 
Melampus (D.) floridanus, hence justifying 
putting Conrad's name in synonymy with De- 
tracia. 

Anatomical comparison of Detracia with 
Melampus does not justify their generic sep- 
aration. Thus Detracia is treated as a subge- 
nus of Melampus [see the remarks under 
Melampus s. I.]. 

The subgenus Detracia is represented in 
the West Indian region by five species, which 
can be distinguished on the basis of shell 
morphology. The type species, Melampus 
(D.) bullaoides, is usually high spired, oval- 
elongate and without any indication of a ca- 
rina on the shoulder of the body whorl. The 
spire has axial ribs and incised spiral 
grooves, and in juveniles it is hirsute. The 
spire of juvenile Melampus (D.) monile is also 
hirsute (Figs. 341 , 345), but the shell is ovate- 
conic and the middle riblets of the outer lip 
are the strongest, whereas in Melampus (D.) 
bullaoides the anteriormost riblet of the outer 
lip is strongest. Some high-spired specimens 
of North American Melampus (D.) floridanus 
resemble Melampus (D.) bullaoides, but can 
be distinguished from them by the absence 
of axial ribs and hairs on the spire, as well as 
by the conspicuous parietal callus that occu- 
pies the site of the anterior parietal tooth. 
This latter character also distinguishes 
Melampus (D.) floridanus from its South 
American counterpart, Melampus (D.) para- 
nus, which lacks the parietal callus. In addi- 
tion, the South American species never has 
more than three riblets in the outer lip, 
whereas the North American species has four 
to eight riblets. Also included in this subge- 
nus is Melampus (D.) morrisoni, a species 
that has certain characteristics of Melampus 
s. s., such as the readily visible upper parietal 
tooth and a discrete anterior parietal tooth. 
Placement in Detracia is based upon the 
strong columellar tooth, narrow aperture, 
long palliai gonoducts and the pouch-like 
mantle organ. 

Habitat: The West Indian species of Detracia 
characteristically live farther from the water 
than do the species of Melampus s.s. with 
which they can occur. Melampus (D.) monile 
is an exception in preferring the area of the 
high-tide mark, in which it is very common 
among piles of rocks frequently covered by 
waves at high tide. Melampus (D.) morrisoni 



prefers inland lagoons and, along with 
Melampus (D.) bullaoides, lives in areas 
reached only by spring tides. The North 
American Melampus (D.) floridanus and the 
South American Melampus (D.) paranus are 
very closely related. Morrison (1951a) inter- 
preted this similarity as a case of parallel ev- 
olution. The North American species lives in 
inland salt marshes of low salinity and curi- 
ously it is absent from mangroves, whereas 
its South American counterpart is a su- 
pratidal estuarine species, living in man- 
groves (Marcus & Marcus, 1965a). 

Range: The subgenus Detracia is mostly 
tropical and occurs in the Indo-Pacific and 
the West Indies. In the Western Atlantic it 
ranges from New Jersey to southern Brazil. 

Melampus (Detracia) bullaoides 

(Montagu, 1808) 

Figs. 290-314 

Voluta bullaoides Montagu, 1808: 102, pl. 30, 
fig. 4 [Lincoln, England (error), herein 
corrected to St. Vincent's, West Indies; 
location of type unknown]. 

Auricula multivolvis Jeffreys, 1 833: 518 [Scar- 
borough, England (error), herein cor- 
rected to St. Vincent's, West Indies; ho- 
lotype USNM 55308 (Fig. 290)]. 

Tornatella bullaoides (Montagu). Férussac, 
1821: 108. 

Melampus bulla Lowe, 1832: 280 [unneces- 
sary new name for Voluta bullaoides 
Montagu]. 

Melampus (Melampus) bulla Lowe. Beck, 
1837: 108. 

Detracia bullaeoides (Montagu). Gray, 1840: 
20 [unjustified emendation for bulla- 
oides]. 

Auricula cingulata Pfeiffer, 1840: 251 [Cuba; 
location of type unknown]; Küster, 1844: 
40, pl. 6, figs. 4-6; Reeve, 1877, pl. 6, fig. 
46. 

Auricula oliva Orbigny, 1841 : 189, pl. 12, figs. 
8-10 [Outskirts of Havana, Cuba; lecto- 
type herein selected BMNH 1854.10.4. 
109 (Fig. 291)]. 

Melampus cingulatus (Pfeiffer). С. В. Adams, 
1849: 42; С. В. Adams, 1851: 186; Shut- 
tleworth, 1854b: 102; Pfeiffer, 1854b 
147; Pfeiffer, 1856a: 17; Binney, 1859 
161, pl. 75, figs. 12, 13; Binney, 1860: 4 
Poey, 1866: 394; Pfeiffer, 1876: 301 
Nevill, 1 879: 219; Arango у Molina, 1 880 
58; Crosse, 1890; 258. 



WESTERN ATLANTIC ELLOBIIDAE 



277 



Conovulus bullaoides (Montagu). Forbes & 
Hanley, 1852: 197. 

Melampus poeyi Pfeiffer, 1853b: 126 [Cuba; 
location of type unknown]; Pfeiffer, 
1854b: 147; Pfeiffer, 1856a: 17; Pfeiffer, 
1876: 301. 

Melampus (Tralia) cingulatus (Pfeiffer). H. & A. 
Adams, 1854: 11. 

Melampus (Tifata) cingulata (Pfeiffer). H. & A. 
Adams, 1855b: 245. 

Melampus bullaoides (Montagu). Pfeiffer, 
1 856a: 1 8; Kobelt, 1 901 : 277, pi. 33, figs. 
6-8. 

Melampus oblongus Pfeiffer, 1856b: 393 
[Bermuda; lectotype Inerein selected 
BMNH 1968848 (Fig. 292)]. 

Tralia cingulata (Pfeiffer). Binney, 1865: 18 
fig. 19; Tryon, 1866: 9, pi. 18, fig. 10 
Fischer & Crosse, 1880: 22; Dall, 1883 
323. 

Melampus ? bullaoides (Montagu). Pfeiffer 
1876: 301. 

Melampus (Detracia) bulloides (Montagu) 
Dall, 1885: 285, pi. 18, fig. 7; Dall, 1889 
92, pi. 47, fig. 7; Simpson, 1889: 68 
Maury, 1922: 56 [misspelling of bulla- 
oides]. 

Melampus bul i moldes (Montagu). Verrill, 
1901: 35 [error for bullaoides]. 

Melampus bulloides (Montagu). Davis, 1904: 
126, pi. 4, fig. 4 [error for bullaoides]. 

Melampus (Detracia) bullaoides (Montagu). 
Peile, 1926: 88. 

Melampus (Detracia) bullaeoides (Montagu). 
Thiele, 1931: 467; Zilch, 1959: 65, fig. 
207 [error for bullaoides]. 

Detracia bulloides (Montagu). M. Smith, 
1937: 147, pi. 55, fig. 1; pi. 67, fig. 7 [pi. 
67 copied from Dall (1885, pi. 18)]; Perry, 
1940: 178: Coomans, 1958: 103; Porter, 
1974: 300 [error for bullaoides]. 

Detracia bullaoides (Montagu). Morrison, 
1951a: 18, figs. 1, 5 [systematics]; Mor- 
rison, 1951b: 9; Perry & Schwengel, 
1955: 198, pi. 53, fig. 359; Morrison, 
1958: 1 18-124 [ecology]; Warmke& Ab- 
bott, 1961: 153, pi. 28, fig. o; Coomans, 
1969: 82; Morris, 1973: 274, pi. 74, fig. 
13; Abbott, 1974: 332, fig. 4092; Hum- 
phrey, 1975: 196, pi. 22, fig. 26; Emerson 
& Jacobson, 1976: 190, pi. 26, fig. 22; 
Rehder, 1981: 648, fig. 349; Gibson- 
Smith & Gibson-Smith, 1 982: 1 1 7; Vokes 
& Vokes, 1 983: 60, pi. 22, fig. 1 5; Jensen 
& Clark, 1986: 457, figured. 

Detracia roquesana Gibson-Smith & Gibson- 
Smith, 1982: 117, fig. 6 [Isla de los 



Roques, Venezuela; holotype USNM 
784718 (Fig. 300)]. 

Description: Shell (Figs. 290-305) to 15 mm 
long, globose to fusiform, solid, shiny, uni- 
form whitish, yellow to brown or with as many 
as three, rarely more, white, unequally wide 
bands on body whorl; body whorl frequently 
with axial zigzag markings or with combina- 
tion of bands and markings. Deep umbilical 
groove sometimes present in gerontic spec- 
imens. Spire high, mucronate, whorls as 
many as 13, flat and sculptured with well- 
marked spiral grooves, axial ribs and a spiral 
row of laterally compressed, short periostra- 
cal hairs. Body whorl 70% of total length, 
oval, smooth or with very faint spiral lines, 
without carina on shoulder. Aperture length 
about 80% of body whorl, very narrow, an- 
gulated anteriorly, with base sometimes 
broad and round in gerontic specimens; inner 
lip with a strong, oblique, twisted columellar 
tooth and a small, oblique, hidden parietal 
tooth just posterior to conspicuous longitudi- 
nal parietal callus; area posterior to parietal 
tooth excavated, with anterior border weakly 
raised to plait-shaped; in the latter case, cor- 
responding riblet of outer lip becomes stron- 
ger, forming wall of narrow anal canal; outer 
lip sharp, rarely smooth within, with one 
strong riblet opposite columellar tooth, usu- 
ally followed posteriorly by as many as eight 
riblets that do not reach the edge of the lip, 
gradually becoming smaller towards poste- 
rior end of aperture. Inner partition of whorls 
occupying entire body whorl; connection of 
posterior visceral mass space with aperture 
very narrow (Fig. 302). Protoconch trans- 
lucent, whitish to slightly brown (Figs. 303- 
305). 

Animal bluish gray; foot dirty white; top of 
neck dark brown to black; tentacles subcy- 
lindric, pointed, translucent in first quarter, 
abruptly changing to dark gray or black; 
mantle skirt light gray. Palliai cavity long; 
mantle organ dark brown, well developed, 
forming very conspicuous pouch; kidney 
long. 

Radula (Figs. 306-310) having formula [24 
+ (1 + 14) + 1 + (14 + 1) + 24] X 100. Base 
of central tooth twice width of base of later- 
al teeth, triangular, with very conspicuous 
prominences on inner surface of arms; crown 
smaller than that of lateral teeth, with medial 
depression at posterior edge; mesocone 
small, sharp; ectocones not defined. Lateral 
teeth ten to 18; crown strong, broadly trian- 



278 



MARTINS 




FIGS. 290-305. 



WESTERN ATLANTIC ELLOBIIDAE 



279 



guiar, half total length of tooth; mesocone 
sharp, pointing laterally; no distinct en- 
docone or ectocone. Transitional tooth with 
base partly reduced, crown weakly project- 
ing posteriorly, with small ectocone or serrate 
edge on ectocone site. Marginal teeth 20 to 
31 with reduced base and elongated crown; 
mesocone strong and sharp, gradually be- 
coming rounded toward the edge of the rad- 
ular ribbon; appearance of ectocones incon- 
sistent from row to row. 

Stomach (Fig. 311) as in subfamily. 

Reproductive system (Fig. 312) with ovo- 
testis conical, dark brown; mucous gland 
spiral, conical; prevaginal caecum very con- 
spicuous; bursa duct thick, enters vagina op- 
posite to exit of posterior vas deferens; bursa 
large, approximately oval; vagina thin, about 
one and four-fifths times length of body whorl; 
penis thin, long; penial retractor inserting with 
columellar muscle. 

Nervous system (Fig. 313) having cerebral 
commissure about as long as width of cere- 
bral ganglion; left parietovisceral connective 
twice the length of right one. 

Remarks: Melampus (D.) bullaoides originally 
was stated to belong to the British fauna al- 
though Montagu (1808) doubted its origin. He 
reported it as from Lincoln, because this was 
the locality given on the lot label in the Port- 
land collection, from which the shell had 
been purchased. Lowe (1832) repeated the 
original information when, for no apparent 
reason, he renamed Montagu's species 
Melampus bulla. Beck (1 837) erroneously re- 
ported Lowe's species from "Atlantic Ocean, 
Boreal Africa." The shell, however, became 
well known in European collections, allowing 
Gray (1840: 21) to remark, "it is one of the 
most common shells in the small boxes from 
the West Indies." Jeffreys (1869: 109) also 
noted that "Voluta bullaoides of Montagu (my 
Auricula multivolvis) [Fig. 290] is a rather 
common West Indian species." He also 



stated that a specimen had been found at 
Scarborough and that the species had been 
reported from Croisic in the Loire-lnferieure. 
Morrison (1951a) explained those odd occur- 
rences as inclusions in ballast picked up by 
ships in the West Indies and dumped along 
the coast of England. 

The high degree of variability that charac- 
terizes the genus Melampus is also notice- 
able in Melampus (D.) bullaoides and caused 
the introduction of most of the names here 
considered synonyms. In Pfeiffer's three ma- 
jor revisions of the family (1854b, 1856a, 
1876), the name Melampus bullaoides ap- 
pears only in the last two, indeed with a query 
in the last one. Pfeiffer (1856a) noted that 
Forbes & Hanley (1852) had treated his 
Melampus cingulatus from Cuba as a junior 
synonym of Montagu's species. Although he 
admitted that they were very closely related, 
Pfeiffer was reluctant to synonymize them 
solely on the basis of Montagu's figure, leav- 
ing the problem, in his words, to the consid- 
eration of the experts. Almost at the same 
time Pfeiffer described Melampus cingulatus, 
Orbigny (1841) described and nicely illus- 
trated Auricula oliva from Cuba (Fig. 291). 
Presumably Orbigny was not aware of Pfeif- 
fer's publication, because the two descrip- 
tions are very similar. The second of Pfeiffer's 
supposed species, Melampus poeyi, also 
from Cuba, is intermediate between Melam- 
pus bullaoides and Pfeiffer's Auricula cingu- 
lata, according to Pfeiffer's observation 
(1856a). The last of Pfeiffer's names, Melam- 
pus oblongus, was applied to a Bermudian 
specimen (Fig. 292) that Pfeiffer (1856b) 
thought was more closely allied to Melampus 
angiostomus (Deshayes, 1831) than to his 
Auricula cingulata. The Bermudian speci- 
mens have a quasi-smooth outer lip, and 
some populations have only the characteris- 
tic strong riblet opposite the columellar tooth 
(Figs. 293-296). Comparison of individuals 
from Bermuda with specimens from Florida 



FIGS. 290-305. Melampus (D.) bullaoides (Montagu). (290) Auricula multivolvis Jeffreys, holotype (USNM 
55308), Scarborough, England, si 7.5 mm. {29^) Auricula oliva Orbigny, lectotype (BMNH 1854.10.4.109), 
Cuba, si 11.0 mm. (292) M. oblongus Pfeiffer, lectotype (BMNH 1968848). Bermuda, si 11.1 mm. (293) 
Somerset Bridge, Bermuda, si 8.1 mm. (294) Hungry Bay, Bermuda, si 10.6 mm. (295) Hungry Bay, 
Bermuda, si 1 0.3 mm. (296) Hungry Bay, Bermuda, sM 1 .2 mm. (297) Crawl Key, Florida (R.B.), si 9.0 mm. 
(298) Big Pine Key, Florida, si 9.4 mm. (299) South Mastic Pt., Andros Island, Bahamas, si 9.1 mm. (300) 
Detracia roquesana Gibson-Smith & Gibson-Smith, holotype (USNM 784718), Isla de los Roques, Vene- 
zuela, sl 10.6 mm. (301) Long Key, Florida, si 2.4 mm. (302) Grassy Key, Florida, si 13.7 mm. (303) Lateral 
view of spire and protoconch, Somerset Bridge, Bermuda. (304) Lateral view of spire and protoconch. Long 
Key, Florida. (305) Top view of spire and protoconch, Somerset Bridge, Bermuda. Scale 1 mm. 



280 



MARTINS 




FIGS 306-309 Melampus (D.) bullaoides, radular teeth. Somerset Bridge, Bermuda, sl 9.0 mm. (306) 
Central and lateral teeth. (307) Transitional and lateral teeth. (308) Marginal teeth. (309) Lateral view of 
marginal teeth in preceding figure. Scale 50 цт. 



WESTERN ATLANTIC ELLOBIIDAE 

с IL 2L 15L T 1M 7M 8M 12M13M 17M 18M 



281 




ûujjjâââooo 



с 1L 2L 11L12LT1M2M 




В 8M9M 15M16M21M22M 



OO pp pt^_ 



FIG. 310. Melampus (D.) bullaoides, radula. A, 
Somerset Bridge, Bermuda; B, Big Pine Key, Flor- 
ida. Scale 10 i-im. 




FIG. 31 1 . Melampus (D.) bullaoides, stomach, Flor- 
ida. Scale 1 mm. 



and Bahamas, however, revealed overlap in 
characters of the apertural dentition (Figs. 
297-299, 301 , 302). One must conclude that, 
owing to its variable expression, the apertural 




FIG. 312. Melampus (D.) bullaoides, reproductive 
system. Grassy Key, Florida. Scale 1 mm. 

dentition in this species is not a reliable tax- 
onomic character and that Melampus oblon- 
gus Pfeiffer from Bermuda is conspecific with 
Melampus (D.) bullaoides. 

Very recently Gibson-Smith & Gibson- 
Smith (1982), on the basis of six beach spec- 
imens, described Detracia roquesana from 
Islas de los Roques, off Venezuela (Fig. 300). 
The Bermudian specimens in my collection, 
which I refer to Pfeiffer's Melampus oblon- 
gus, as well as those from the Bahamas, fit 
the description of Gibson-Smith & Gibson- 
Smith. The brown protoconch, so common in 
Bermudian shells, also occurs in certain 
specimens from Florida, although in the latter 
specimens the aperture is narrower and more 
dentate. Analysis of protoconch, radula and 
anatomy of the Bermudian forms did not 
yield any differences between specimens 
from Florida and those from the Bahamas. 
These facts led me to consider Detracia ro- 
quesana Gibson-Smith & Gibson-Smith a 
junior synonym of Melampus (D.) bullaoides 
(Montagu). 

Melampus (D.) bullaoides is very easily dis- 
tinguished from Melampus (D.) floridanus by 




vg prvc prg piprc 



bg be 



FIG. 313. Melampus (D.) bullaoides, central nervous system, Grassy Key, Florida. Scale 1 mm. 



the presence of ribs on its spire and by its 
protruding, mucronate apex. The spire is 
constricted toward the apex and broadens 
suddenly toward the base. The juveniles have 
a crown of periostracal hairs. The last whorl 
shows a wide range of color patterns, and 
frequently young specimens are brightly col- 
ored. In Melampus (D.) flohdanus the spire is 
regularly conical, glabrous, and the body 
whorl has as many as three chestnut-brown 
bands. 

Habitat: Melampus (D.) bullaoides is a com- 
mon inhabitant of the mangroves and can be 
very abundant in some localities. The species 
prefers the supralittoral zone and it frequently 
lives on the edges of inland tidal lagoons, 
sometimes in relatively dry places, in which 
they aggregate under rocks, pieces of wood, 
cardboard and other decaying trash. 



Range: Bermuda; Florida, West Indies to 
Suriname (Fig. 314). 

Specimens Examined: FLORIDA (USNM 
27914, 39833, 39838, 39839, 1524268, 
492459): Fernandina (USNM 492544); Lake 
Worth at Boynton (ANSP 194770); Miami 
(ANSP 91284; USNM 153399, 492460); Co- 
conut Grove (MCZ 82497, 291238, 291258); 
Virginia Key (MCZ 46880); Bear's Cut, Key 
Biscayne (MCZ 153116); Soldier Key (MCZ 
174459); Third Ragged Key, above Sands 
Key (USNM 462736); Sands Key, Biscayne 
Bay (MCZ 291269); Elliot Key (ANSP 
160894); Key Largo (ANSP 56813; MCZ 
56473, 291255, 291264; USNM 68130, 
492546, 597456); Tavernier (MCZ 153121); N 
of Tavernier Key (A.M.); Tavernier Key 
(USNM 492550); Snake Creek (MCZ 291 058); 
Plantation Key (MCZ 199343, 291057); S of 



WESTERN ATLANTIC ELLOBIIDAE 



283 




FiG. 314. Melampus (D.) bullaoides, geographic 
distribution. 



Ocean Drive, Plantation Key (A.M.); Indian 
Key (USNM 462895, 492547); Indian Key Fill, 
N of Indian Key Channel (A.M.); Little Duck 
Key (MCZ 291061); Lower Matecumbe Key 
(USNM 700771); N end of Long Key (A.M.); 
Bonefish Key (MCZ 291059); Upper Grassy 
Key (MCZ 291051); Grassy Key (MCZ 
291064; A.M.); Crawl Key (MCZ 174470, 
199342, 291046, 291047; A.M.); Key Vaca 
(ANSP 181137); Marathon (MCZ 153258); 
Knight Key (A.M.); Bahia Honda Key (ANSP 
88030, 88132, 104098, 189562; USNM 
269780); Howe Key (USNM 681640, 706766) 
Big Pine Key (ANSP 89549, 104099, 189559 
MCZ 250733, 291048, 291049, 291517 
USNM 597454); Long Beach Drive, Big Pine 
Key (A.M.); VV end of Kohen Avenue, Big Pine 
Key (A.M.); Big Torch Key (ANSP 104100; 
A.M.); Little Torch Key (MCZ 291053); Ram- 
rod Key (MCZ 291050, 291247); Sugarloaf 
Key (ANSP 9635, 22475, 89550, 189560); 
Lower Sugarloaf Key (USNM 672440); Sum- 
merland Key (USNM 270318); West Summer- 
land Key (MCZ 291084; A.M.); Military Key 
(MCZ 291055); Pavilion Key (ANSP 93434); 
Boca Chica Key (ANSP 104097, 152502, 
189561; MCZ 162638; USNM 270327); Cow 
Key (USNM 596786); Stock Island (ANSP 
149994; USNM 270280); Key West (ANSP 



56812, 100848, 174635, 264540, 294310; 
USNM 36015, 36965, 61101, 153076, 
270363, 338357); Snake Key (ANSP 1 05461); 
Seminole Point (ANSP 105437); Boca 
Grande Key (USNM 272834); Flamingo Key 
(MCZ 291060); Cape Sable (MCZ 291062); 
Marco Key (USNM 381333); mouth of Hend- 
erson Creek, 5 km N of Marco (MCZ 29421 5); 
Little Marco (ANSP 93435); Bonita Springs 
(MCZ 291063); Carl E. Johnson Park, Little 
Carlos Pass (A.M.); Mound Key (MCZ 
291270); Punta Passa (MCZ 13705, 291056); 
Sanibel Island (ANSP 179352; MCZ 291 052); 
Tarpon Bay, Sanibel Island (MCZ 13704, 
55961); Turner's Pond, Sanibel Island (MCZ 
232526); E of St. James, Pine Island (ANSP 
93433); Captiva Island (ANSP 149406; MCZ 
60186, 236852, 291054); Osprey (ANSP 
88078); Mullet Key (USNM 652407; A.M.); 
Pinellas Point (MCZ 294209); Bayou off Gulf- 
port (MCZ 138942); St. Petersburg (MCZ 
291242; USNM 343843, 366191, 466193); 
Maximo Point, St. Petersburg (ANSP 
167540); Shell Bay, off St. Petersburg (USNM 
466207, 466289); Sand Key (ANSP 129249; 
USNM 338365); Harts Bayou, Boca Ciega 
Bay (MCZ 291266); Indian Rocks (ANSP 
167541); Clearwater Island (ANSP 189558); 
Clearwater (USNM 61 1 785); Cedar Key (MCZ 
291246; USNM 36895, 37611, 37612). BER- 
MUDA: (ANSP 85590; MCZ 24246, 291240, 
291253, 291260, 291262, 292267; USNM 
6529, 94435, 98153, 173651, 492543); 
Hamilton (ANSP 182551; USNM 152145, 
171960); Fairyland (ANSP 99058, 111095); N 
end of Long Bird Bridge (A.M.); Hungry Bay 
(ANSP 88581; A.M.); S end of Ely's Harbour 
(A.M.); W side of Somerset Bridge (A.M.); 
Mangrove Bay (A.M.); Ireland Island (USNM 
712379); Pond W of Evans Bay (A.M.); Rid- 
dell's Bay (USNM 621666). BAHAMA IS- 
LANDS (MCZ 24141): GRAND BAHAMA IS- 
LAND: Dead Mans Reef [Sandy Bevan's Cay] 
(ANSP 371222); Riding Point (ANSP 371520, 
375562); 4 km NW of Sweetings Cay Light 
(ANSP 307628); GREAT ABACO ISLAND: 
Witch Point (ANSP 299481, 359153; USNM 
492580c); Crossing Bay (ANSP 173189); 
McLeans Town (ANSP 369066); Running 
Mon Canal (ANSP 369777); North Hawksbill 
Creek (ANSP 370565); BIMINI ISLANDS: Al- 
icetown, Norlh Bimini (USNM 598841); oppo- 
site Cat Tail Pond, South Bimini (ANSP 
325782); BERRY ISLANDS: Chub Cay (ANSP 
359148); Frazier, Hog Cay (ANSP 194182, 
195213); ANDROS ISLAND (ANSP 226713; 
USNM 269844); Stafford Creek (ANSP 



284 



MARTINS 



151848, 151930); Mangrove Cay (MCZ 
24102; USNM 180518); Bastion Point, Man- 
grove Cay (USNM 269226, 269252); Rocky 
Point, Mangrove Cay (USNM 270214, 
270215); Solomon Pond, Mangrove Cay 
(USNM 269968); 5 km from mouth of Lisbon 
Creek, Lindsey Creek (USNM 270234); First 
island off Mintie Bar, SE of South Bight 
(USNM 271785); Long Bay Key (USNM 
269323); PARADISE ISLAND (A.M.); NEW 
PROVIDENCE ISLAND (ANSP 18485, 
299646; USNM 124376): Nassau (MCZ 
107498; USNM 160767, 467111); Bar Point 
(A.M.); Delaporte Point (A.M.); W of Rock 
Point (A.M.); Clifton Point (A.M.); Clifton Pier 
(A.M.); shore off Millars Road (A.M.); Millars 
Sound by Bacardi Road (A.M.); Bonefish 
Pond (A.M.); South Beach (MCZ 291268); 
Malcolm Creek (A.M.); Dick's Point (MCZ 
291518); ROYAL ISLAND (MCZ 184098, 
280395; USNM 343844, 366190, 468116); 
ELEUTHERA ISLAND (USNM 465988): Tar- 
pon Bay (MCZ 135934, 175921); Great Oys- 
ter Pond (MCZ 291265); BRIGADINE KEY 
(USNM 270034); CAT ISLAND: Arthurstown 
(MCZ 291237); LONG ISLAND: Simms (MCZ 
291251); Galloway's Landing (MCZ 291241); 
Pinders (MCZ 113328); AKLINS ISLAND: 
Pinnacle Point (USNM 390857); ROOKER KEY 
(USNM 390663, 390674a); GREAT INAGUA: 
Mafthewstown (MCZ 291263); 5 km SE of 
Mafthewstown (MCZ 190050); CAY SAL 
BANK: Cay Sal, (MCZ 291256); Salt Lagoon, 
Cay Sal (USNM 51 3426). TURK'S & CAICOS: 
CAICOS ISLAND: Bell Cay (USNM 391323). 
CUBA (ANSP 56810, 567800; MCZ 31418, 
291257, 294214; USNM 10966, 39840, 
55727, 336072, 492461): Cayo Juan Garcia 
(MCZ 291271); La Habana (MCZ 291259) 
Cayo Birricu, N. of Habana (ANSP 362823) 
Cayo Blanco, Cárdenas Bay (ANSP 157955) 
Playa del Bellamar (MCZ 291239, 291243) 
Cayo Cristo (MCZ 292559); Caibahén (MCZ 
291248, 294213); Dimas (USNM 492559b); 
Cayo Romano (MCZ 291272); Punta de Pie- 
dra (MCZ 291252); Santa Cruz del Sur (MCZ 
131939, 291254); Santa Maria Key (MCZ 
291261); Cochinos Bay (USNM 492548); 
Cayo de las Cinco Léguas (ANSP 158053); 
Finca, Sabanalmar (MCZ 294210); Isla de Pi- 
nos (MCZ 48081). JAMAICA (ANSP 56811; 
MCZ 291245; USNM 94746, 374270a. 
492462, 492551): Montego Bay (ANSP 
359146); Kingston (USNM 442736); Harbor 
Head, Kingston (USNM 617127); Hunt's Bay 
(USNM 441719); Cow Bay (USNM 440985); 
Palisadoes (USNM 442465); Port Royal 



(USNM 442419); Rock Fort (USNM 374243); 
Great Goat Island (ANSP 359156). HAITI 
(ANSP 146738): St. Louis (USNM 439392); 
Gonave Island (MCZ 82118; USNM 380256); 
near Port-au-Prince (USNM 403034, 403035, 
440610a); île-à-Vache, Soulette Bay (USNM 
439169a, 439169b, 442850a); Port Salut 
(USNM 403760); Aquin (USNM 403256, 
403573, 440170); Bizoton (USNM 439828). 
DOMINICAN REPUBLIC: Monte Cristi (MCZ 
291249). PUERTO RICO: Punta Arenas, N of 
Joyuda (A.M.). VIRGIN ISLANDS: ST. CROIX 
(ANSP 56809). LESSER ANTILLES: AN- 
GUILLA BANKS (MCZ 294216); ANTIGUA: 
Fitches Creek (USNM 809737); BARBUDA 
(USNM 735816). CARIBBEAN ISLANDS: 
CAYMAN ISLANDS: Cayman Brae (MCZ 
294212); Georgetown Barcadero, Grand 
Cayman (ANSP 209770). COLOMBIA (MCZ 
291273). VENEZUELA: Islas de los Roques 
(USNM 784718). SURINAME: Paramaribo 
(MCZ 274063). 

Melampus (Detracia) floridanus 

Pfeiffer, 1856 

Figs. 315-318, 321-332 

Melampus (Tralia) floridianus Shuttieworth. H. 
& A. Adams, 1854: 11 [nomen nudum]. 

Melampus floridanus Shuttieworth. Pfeiffer, 
1854b: 147 [nomen nudum]. 

Tralia (Tifata) floridana Shuftieworth. H. & A. 
Adams, 1855b: 245 [nomen nudum]. 

Melampus floridanus "Shuttieworth" Pfeiffer, 
1856a: 35 [Florida, herein restricted to 
Муакка River; location of type un- 
known]; Binney, 1860: 4; Nevill, 1879: 
219; Dall, 1885: 281, pi. 18, fig. 2; Dall, 
1889: 92, pi. 47, fig. 2; Simpson, 1889: 
68; Kobelt, 1898: 213, pi. 24, fig. 14; Hin- 
kley, 1907: 71; Maury, 1922: 55; С W. 
Johnson, 1934: 159; M. Smith, 1937: 
146, pi. 55, fig. 5, pi. 67, fig. 2 [pi. 67 from 
Dall (1885)]. 

Melampus floridianus Shuttieworth. Binney, 
1 859: 1 65 [error for floridanus; pi. 75, fig. 
30 is of Melampus (M.) bidentatus Say 
(Fig. 265)]. 

Tralia floridana (Shuttieworth) (Pfeiffer). Bin- 
ney, 1 865: 1 6 [fig. 1 7 is of Melampus (M.) 
bidentatus]; Tryon, 1866: 9 [pi. 18, fig. 11 
copied from Binney (1859) shows 
Melampus (M.) bidentatus]. 

Detracia floridana (Pfeiffer). Morrison, 1951a: 
17, figs. 4, 7 [description, habitat]; Mor- 
rison, 1954: 15-16 [egg masses); Morri- 
son, 1959: 25 [early life history]; Burch, 



WESTERN ATLANTIC ELLOBIIDAE 



285 



1960a: 182, pl. 1, figs. 2, 91 [chromo- 
somes]; Abbott, 1974: 332 [Fig. 4093 
copied from BInney (1859) is of Melam- 
pus (M.) bidentatus]; Emerson & Jacob- 
son, 1976: 191, pl. 26, fig. 23; Heard, 
1982: 20, fig. 16. 

Detracia floñdana (Shuttleworth). Morrison, 
1951b: 8. 

Melampus floridanus Pfeiffer. Holle & Dineen, 
1959: 50 [systematics]. 

Description: Shell (Figs. 315-318, 321-323) 
to 7 mm long, globose to fusiform, thin, 
smooth to corrugated, dark brown with gray- 
ish tones, with as many as three chestnut- 
brown bands on upper half of body whorl. 
Spire moderately high, mucronato, with as 
many as 10.25 flat, compressed whorls, with 
fine, spirally arranged pits. Body whorl 70% 
of total length, oval to subcylindric, lacking 
carina on shoulder, smooth or with very faint 
spiral lines. Aperture narrow, about 90% of 
length of body whorl, weakly canaliculate at 
base; inner lip with oblique columellar tooth, 
conspicuous parietal callus and, above it and 
hidden inside, small horizontal parietal tooth; 
outer lip sharp, with as many as ten subequal 
riblets, not reaching edge. Inner partition of 
whorls occupying entire body whorl (Fig. 
316). Protoconch raised, smooth, translu- 
cent, dark brown (Figs. 321-323). 

Animal bluish gray; foot paler; tentacles 
subcylindric, pointed, darker toward tip; 
mantle skirt grayish. Mantle organ dark 
brown, well developed, forming conspicuous 
pouch. 

Radula (Figs. 324-328) having formula 
[14 + (1 +12)+1 + (12 + 1) + 14] X 100. Central 
tooth with base wider than that of lateral 
teeth, with conspicuous medial promi- 
nences; crown half length and width ofthat of 
lateral teeth, rounded posteriorly; mesocone 
sharp; ectocones well marked, small. Lateral 
teeth 11 to 16; crown strong, half total length 
of tooth; mesocone sharp, pointing laterally; 
ectocone well developed in all lateral teeth. 
Transitional tooth with very weak endocone. 
Marginal teeth 13 to 17, with reduced base 
and elongate crown; mesocone becoming 
shorter and thinner; endocone and second 
cusp of ectocone in first marginal tooth; outer 
edge of base assuming configuration of den- 
ticle around third marginal tooth, first cusp of 
ectocone becoming smaller and third cusp of 
ectocone appearing; second cusp of en- 
docone appearing on fifth to sixth marginal 
tooth; eighth to tenth marginal teeth without 



additional cusps; last two marginal teeth ru- 
dimentary. 

Digestive system as in Melampus s. s.; 
stomach elongate, muscular band thick (Fig. 
329). 

Reproductive system (Fig. 330) with 
ovotestis shallow-conical, dark brown; albu- 
men gland spiral, conical; fertilization cham- 
ber forming double pouch; vagina and asso- 
ciated vas deferens muscular, long; bursa 
duct entering vagina opposite exit of poste- 
rior vas deferens; penis muscular, long; 
length of anterior vas deferens 75% that of 
penis. 

Nervous system (Fig. 331) having cerebral 
commissure about as long as width of cere- 
bral ganglion; left pleuropedal connective 
very short; left parietovisceral connective 
longer than right one. 

Remarl<s: The name Melampus floridanus ap- 
peared in published lists for several years be- 
fore Pfeiffer (1856a) validated it with a de- 
scription in his Monographia. Holle & Dineen 
(1959) stated that the original specimens had 
been collected in Florida by a Mr. Rugel for 
Shuttleworth, who deposited them in the 
Cuming collection under his manuscript 
name. Pfeiffer (1856a) probably had seen 
these specimens marked as Auricula f leridana 
by Shuttleworth, and also the specimens in 
the Albers collection marked as Auricula rugeli 
by Charpentier. Both names are referred to as 
manuscript names in Pfeiffer's description. 
He gave the measurements of the specimen 
he used for the description, however, men- 
tioning that it was Nr. 1 5 of his collection. The 
type material therefore should include only 
the specimen in Pfeiffer's collection, because 
there is no assurance that Pfeiffer used other 
collections in writing the description. Most au- 
thors have given credit erroneously to Shut- 
tleworth for introduction of Melampus (D.) flo- 
ridanus but in accord with the ICZN Pfeiffer 
must be credited with this name, for it is he 
who validly introduced it. 

According to Morrison (1951a), Binney 
(1859), using shells collected by Bartlett from 
the Florida Keys, wrongly illustrated this spe- 
cies by using an example of a dwarf Melam- 
pus (M.) bidentatus (Fig. 265). Several subse- 
quent authors, including Abbott (1974), 
perpetuated Binney's mistake by copying 
that figure. Morrison (1951a), Emerson & Ja- 
cobson (1976) and Heard (1982) correctly il- 
lustrated Melampus (D.) floridanus, however. 

Melampus (D.) floridanus can be d istin- 



286 



MARTINS 




FIGS. 315-323. 



WESTERN ATLANTIC ELLOBIIDAE 



287 




FIGS. 324-327. Melampus (D.) floridanus, radular teeth. (324-326) Myakka River, Florida, sl 6.7 mm. (327) 
Woodville, North River, North Carolina, sl 5.3 mm. Scale, Fig. 324, 50 цт; all others, 100 |.im. 



guished from Melampus (M.) bidentatus, with 
which it commonly associates, by its smaller 
size, stronger columellar tooth, the callus on 
the site of the first parietal tooth, its narrower 
aperture and more numerous whorls. The 
specimens of Melampus (D.) floridanus from 
southern and western Florida are smooth and 
sometimes brightly colored, and usually re- 
tain all the whorls of the spire, whereas north- 
ern specimens are thinner and corrugated, 
with the apex greatly eroded. 

Habitat: Melampus (D.) floridanus lives in salt 
marshes and freshwater riverbanks on which 
it often occurs with Melampus (M.) bidenta- 
tus. The Floridian salt-marsh snail prefers 
that zone of the marsh rarely flooded by 



spring tides. The animals frequently live half- 
buried in the sediment, against the base of 
the stems of Spartina, Juncus and other 
marsh plants. Very common in some places, 
they were estimated by Morrison (1951a) to 
attain a density of about four billion individu- 
als in a square mile. 

Range: New Jersey to Florida, and along the 
Gulf Coast to Vera Cruz, Mexico (Fig. 332). I 
have not observed specimens from the Flor- 
ida Keys. 

Specimens Examined: NEW JERSEY: Divid- 
ing Creek (A.M.); Newport (ANSP 294331). 
DEIJ\WARE: Woodland Beach (USNM 
522268); Bombay Creek (USNM 473356, 



FIGS. 315-323. Melampus (Detracia). (315) M. (D.) floridanus Pfeiffer, Woodville, North River, North Caro- 
lina, sl 5.2 mm. (316) M. (D.) floridanus, Woodville, North River, North Carolina, sl 5.5 mm. (317) M. (D.) 
floridanus, Myakka River, Florida, sl 6.7 mm. (318) M. (D.) floridanus, Myakka River, Florida, sl 5.7 mm. (319) 
Detracia parana Morrison, holotype (USNM 594591), Para, [Belém]. Brazil, sl 6.5 mm. (320) Auricula glob- 
ulus Orbigny, lectotype (BMNH 1854.12.4.243), Guayaquil, Ecuador, sl 8.1 mm. (321-323) M. (D.) florida- 
nus, lateral and top views of spire and protoconch, Myakka River, Florida. Scale 1 mm. 



288 MARTINS 

C1L2L3L12LT 1М 2M3M4M 




8М 9М ЮМ 11М12М 13М 





FIG. 328. Melampus (D.) florídanus, radula, Cres- 
cent, Georgia. Scale 10 цт. 



^'^- 




FIG. 329. Melampus (D.) floridanus, stomach, 
Georgia. Scale 1 mm. 



628864, 628865, 628866); Augustine Pier 
(ANSP 89556; MCZ 294219; USNM 492587). 
MARYLAND: Morgan Creek, Charlestown 
(MCZ 200469); Mayo Beach (USNM 522289); 
Galesville (USNM 595601); Chesapeake 
Beach (USNM 473812); Parkers Creek 
(USNM 536708); N of Benedict, Patuxent 
River (USNM 473459, 473460, 473461); 
Benedict (USNM 473463); Kepplers, 
Broomes Island (USNM 473466); Helen 
Creek, N of Solomons Island (USNM 
600764); Solomons Island (USNM 4240410; 
Millstone Landing, mouth of Patuxent River 
(USNM 521877); Cobb Island, Potomac River 




FIG. 330. Melampus (D.) floridanus, reproductive 
system, Sapelo Island, Georgia. Scale 1 mm. 



prvc pc pg pig epic cpc eg 




FIG. 331 . Melampus (D.j floridanus, central nervous 
system, Sapelo Island, Georgia. Scale 1 mm. 

(USNM 473565, 473566, 499520, 522920); 
Bretton Bay, Potomac River (USNM 628901); 
Chapel Point, Potomac River (USNM 
758317); opposite Chestertown (ANSP 
106973); Town Point (MCZ 46419); Head of 
Little Choptank River, Cambridge (USNM 
348955); Cambridge (MCZ 52355, 291275); 
Dailsville (ANSP 1332468, 303357; MCZ 



WESTERN ATLANTIC ELLOBIIDAE 



289 







1: 


^ 






.j 


{ 




■ 




''4 













^^^ 








\ 




^^ 


^ 






\ 




7 






/ 


^ 





FIG. 332. Geographie distributions, Melampus (D.) 
floridanus (circles), Melampus (D.) paranus (stars). 
Open symbols, localities from literature. 



55922); Chambers Farm, Dailsville (ANSP 
65100); Whitehaven (MCZ 291276); East of 
Dames Quarter (USNM 618923). VIRGINIA: 
Colonial Beach, Potomac River (USNM 
473890, 473891); Potomac Beach (USNM 
473901, 473902, 473903); Poropotank River 
(USNM 679376); 2 mi NE of Bartlett (USNM 
595938); Yorktown (USNM 474078); Norfolk, 
Lafayette River (USNM 667496). NORTH 
CAROLINA: Cedar Island (A.M.); Williston 
(A.M.); Woodville, North River (A.M.); Beau- 
fort (MCZ 294261; USNM 678946); Morton's 
Hill, near Beaufort (USNM 621431). SOUTH 
CAROLINA: Yemassee (A.M.). GEORGIA: 
Crescent (A.M.); Fort King George, at Darien 
(USNM 628867). FLORIDA: Jacksonville 
(ANSP 132461); Clear Lake (MCZ 294218; 
USNM 30210); Miami (ANSP 77039; USNM 
153403); Everglades fork of Miami River 
(ANSP 82852); Biscayne Bay (USNM 
492586); Seminole Point (ANSP 293554); 
Flamingo Key (MCZ 291041); Cape Sable 
(MCZ 291039); Turner River, near Chokolos- 
kee (ANSP 93436); Everglades City (MCZ 
291 040, 294262); Naples (MCZ 291 041 ); Fort 
Myers (ANSP 62805; MCZ 291277; USNM 
492585); Little Gaspanlla Island (ANSP 
142169); Myakka River (A.M.); Sarasota Bay 



(ANSP 294332; USNM 30624); Big Bend 
Road, Tampa Bay (A.M.); Tampa (ANSP 
76114; MCZ 70562; USNM 37608, 504488); 
Ballast Point, Tampa (MCZ 13815); Hudson 
(A.M.); Tributary to Hudson Bayou (USNM 
487336); Aripeka (ANSP 73901; USNM 
149953); Little Blind Creek, below mouth of 
Chassahowitzka River (ANSP 148526); Tar- 
pon Springs (MCZ 291274); Suwannee River 
(ANSP 189567); St. Marks (ANSP 56815, 
56816). ALABAMA (USNM 492588): SE of 
Heron Bay (ANSP 315714); Mobile (MCZ 
68065); Coden Beach (USNM 422365). 
MISSISSIPPI: Point Cadet, Biloxi (USNM 
518640); Davis Bayou, Ocean Springs 
(USNM 778280); Escatawpa River (ANSP 
315718). LOUISIANA: New Orleans (USNM 
119495). MEXICO: Tampico (ANSP 46584); 
Rio Vinazco (USNM 675265); SE of Tuxpan, 
Vera Cruz (USNM 675272). 

Melampus (Detracia) paranus 

(Morrison, 1951) 

Figs. 319, 332, 333 

Detracia parana Morrison, 1951a: 19, fig. 3 
[Amazon River at Para, Brazil; holotype 
USNM 594591 (Fig. 319); three para- 
types USNM 32090]; Morrison, 1951b: 9; 
Marcus & Marcus, 1965a: 42-51, figs. 
19-21, 23-25 [distribution, ecology, 
anatomy]; Rios, 1970: 138; Rios, 1975: 
158, pi. 48, fig. 766. 

Melampus (Detracia) paranus (Morrison). Al- 
tena, 1975: 86. 

Description: Shell (Fig. 319) to 7 mm long, 
globose to fusiform, thin, smooth, yellowish 
brown with one to three darker brown bands 
on body whorl, the one nearest suture more 
conspicuous. Spire low, with as many as ten 
flat whorls, dark brown with lighter band. 
Body whorl 80-90% of shell length, fusiform 
to subcylindric, without hint of carina on 
shoulder. Aperture 85-90% of length of body 
whorl, narrow, weakly canaliculate at base; 
inner lip with strong, oblique columellar tooth 
and small, horizontal parietal tooth hidden in- 
side aperture; outer lip sharp, usually with 
one riblet opposite columellar tooth, some- 
times with none, rarely with two or three. 

Animal with tentacles bulbous at base; 
eyes surrounded by unpigmented skin. Vis- 
ceral mass separated from foot by one whorl, 
with corresponding extension of mantle cav- 
ity; mantle organ forming funnel-shaped 
pouch. 



290 



MARTINS 




FIG. 333. Melampus (D.) paranus (Morrison), rad- 
ula, Cananeia, Brazil; redrawn from Marcus & Mar- 
cus (1965a). Scale 10 |дт. 



Radula (Fig. 333) having formula 
[16 + 16 + 1 + 1 6 + 1 6] X 1 00. Base of central 
tooth weakly concave, not emarginate; 
crown rounded posteriorly; mesocone small, 
rounded; ectocones absent. Mesocone of 
lateral teeth about half of length of tooth, with 
conspicuous ectocone. Endocone appearing 
on second marginal tooth; as many as five 
ectocones on marginal teeth. 

Remarks: Melampus (D.) paranus was de- 
scribed by Morrison (1951a) on the basis of 
four specimens in the United States National 
Museum of Natural History, collected in Bra- 
zil before 1885. Only the type specimens 
were available to me and they constitute the 
basis for my description of the shell. All data 
on the animal and its anatomy were taken 
from Marcus & Marcus (1965a). In their study 
of 174 specimens from Cananeia, Brazil, 
Marcus & Marcus observed the aperture 
length to be barely 75% of the length of the 
body whorl, an important difference from the 
few specimens that constitute the type ma- 
terial. I observed similar variation in the North 
American companion species Melampus (D.) 
floridanus. 

According to Morrison (1951a) the strong 
similarities between Melampus (D.) paranus 
and Melampus (D.) floridanus suggest that 
both species underwent closely parallel evo- 
lution. The former differs from the North 
American species by its lack of a callosity 
above the columellar tooth and by the num- 
ber of riblets inside the outer lip. Marcus & 
Marcus (1 965a) observed that Melampus (D.) 
paranus commonly had one riblet, seldom 
none and rarely two, and only one of the 1 74 
specimens examined had three riblets inside 
the outer lip. Melampus (D.) floridanus has 
four to ten riblets inside the outer lip. 

Habitat: According to Marcus & Marcus 
(1965a), Melampus (D.) paranus is a supralit- 
toral estuarine species that lives in man- 
groves together with Melampus (M.) coffeus. 



Range: Suriname (Altena, 1975), south to 
Cananeia, Brazil (Marcus & Marcus, 1965a) 
(Fig. 332). 

Specimens Examined: BRAZIL; Para [Belém], 
on the Amazon River (USNM 32090, 594591). 

Melampus (Detracia) monile 

(Bruguière, 1789) 

Figs. 334-354 

Bulimus monile Bruguière, 1789; 338 [West 
Indies, herein restricted to San Juan, Pu- 
erto Rico; location of type unknown]; 
Dillwyn, 1817; 506 [erroneously stated 
as a probable variety of Voluta flava 
Gmelin, 1791]; Cuvier, 1817; 414. 

Melampa monile (Bruguière). Schweigger, 
1820; 739. 

Auricula monile (Bruguière). Férussac, 1821: 
105; Lamarck, 1822; 141; Küster, 1844: 
30, pi. 4, figs. 7-9. 

Auricula monile Lamarck. Menke, 1830; 36; 
Gould, 1833: 67; Jay, 1839; 59; Reeve, 
1842; 106, pi. 187, fig. 8. 

Melampus monile Schweigger. Lowe, 1832: 
292. 

Conovulus monile (Bruguière). Deshayes, 
1836; 71, pi. 27, figs. 5, 5a. 

Melampus (Melampus) monile (Bruguière). 
Beck, 1837; 108. 

Auricula monile Férussac. Potiez & Michaud, 
1838; 202. 

Melampus coronatus С В. Adams, 1849; 41 
[Jamaica; lectotype chosen by Johnson 
& Boss (1972) MCZ 186029 (Fig. 342); С 
В. Adams, 1851; 186; Pfeiffer, 1854b: 
147; Pfeiffer: 1856a: 51; Johnson & 
Boss, 1972: 196, pi. 41, fig. 5 [lectotype 
figured]. 

Melampus flavus Gmelin of authors. С В. Ad- 
ams, 1849; 42; С. В. Adams, 1851; 186; 
H. & A. Adams, 1854; 9; Pfeiffer, 1854b: 
147; Pfeiffer, 1856a; 21; Binney, 1859: 
167, text fig.; Binney, 1860; 4; Binney, 
1865: 12, fig. 14; Tryon, 1866; 8, pi. 18, 
fig. 6; Poey, 1866; 394; Pfeiffer, 1876: 
303; Mörch, 1878: 5; Arango y Molina, 
1880; 59; Dali, 1883; 322; Dali, 1885; 
281, pi. 18, fig. 1; Dali, 1889; 92, pi. 47, 
fig. 1; Simpson, 1889: 68; Crosse, 1890: 
258; Davis, 1904; 126, pi. 4, fig. 5; Peile, 
1926; 88; Maury, 1922; 55; С W. 
Johnson, 1934; 159; M. Smith, 1937: 
146, pi. 55, fig. 12, pi. 67, fig. 1 [pi. 67 
copied from Dall (1885)]; Holle & Dineen, 
1959: 28-35, 46-51. Non Gmelin, 1791. 



WESTERN ATLANTIC ELLOBIIDAE 



291 



Melampus torosa Mörch, 1852: 38 [Antilles; 
location of type unknown]. 

Melampus fusca Mörch, 1852: 35 [Antilles; 
location of type unknown]. 

Melampus coronulus С В. Adams. H. & A. 
Adams, 1854: 10 [error for coronatus]. 

Melampus monilis Lamarck. Shuttleworth, 
1854b: 102; Shuttleworth, 1858: 73 [un- 
justified emendation of monile]. 

Melampus monile Lamarck. Mörch, 1878: 5. 

Melampus flavus (Gmelin?) Binney. Dall & 
Simpson, 1901: 368, pi. 54, fig. 9. Non 
Gmelin, 1791. 

Melampus flavus var. purpureus Davis, 1904: 
126, pi. 4, fig. 6 [Bermuda, herein re- 
stricted to South Shore; lectotype se- 
lected by Baker (1 964) ANSP 86922 (Fig. 
336). 

Melampus flavus var. albus Davis, 1904: 126, 
pi. 4, fig. 7 [Hungry Bay, Bermuda; lec- 
totype selected by Baker (1964) ANSP 
86924 (Fig. 337)]. 

Pira monile (Bruguière). Morrison, 1951b: 8; 
Morrison, 1958: 118-124 [ecology]; 
Nowell-Usticke, 1959: 88; Morrison, 
1964: 119-121 [systematics]. 

Melampus monile (Bruguière). Warmke & Ab- 
bott, 1961: 153, pi. 28, fig. p; Rios, 1970: 
138; Morris, 1973: 273, pi. 74, fig. 9; Em- 
erson & Jacobson, 1976: 192, pi. 26, fig. 
27; Rehder, 1981: 647, fig. 363. 

Melampus (Pira) monilis (Bruguière). Abbott, 
1974: 332, fig. 4090: Rios, 1975: 158, pi. 
48, fig. 765; Gibson-Smith & Gibson- 
Smith, 1982: 116, figs. 2, 3; Vokes & 
Vokes, 1983: 60, pi. 22, fig. 14. 

Melampus (Pira) monile (Bruguière). Hum- 
phrey, 1975: 196, pi. 22, fig. 23 [shell fig- 
ured seems to be Melampus coffeus]. 

Melampus monilis (Bruguière). Cosel, 1978: 
216; Mahieu, 1984: 314; Jensen & Clark, 
1986: 457, figured. 

Description: Shell (Figs. 334-345) to 16 mm 
long, ovoid to fusiform, solid, shiny, usually 
a uniform purplish brown or with as many 
as three narrow white bands, rarely uniform- 
ly white or yellowish. Excavated umbilical 
groove sometimes present in gerontic spec- 
imens. Spire low to moderately high, with as 
many as 1 1 .25 flat whorls, with two or three 
well-marked spiral grooves on first two 
whorls, one or two rows of elongated pits on 
remaining whorls; spiral row of short, laterally 
compressed periostracal hairs, often running 
along spiral row of pits in adult specimens; 
location of hairs does not correspond to that 



of pits. Body whorl averaging 83% of shell 
length, conic to ovoid, smooth or with pitted 
and sometimes carínate shoulder. Aperture 
about 90% length of body whorl, narrow, an- 
teriorly angulate; inner lip with strong, ob- 
lique, twisted columellar tooth, conspicuous 
pahetal callus and, just posterior to it, deep 
parietal tooth; outer lip sharp, with as many 
as ten subequal riblets not reaching edge. 
Inner partition of whorls occupying two- 
thirds of body whorl (Fig. 340). Protoconch 
translucent, brownish (Figs. 343-345). 

Animal bluish gray; foot whitish; top of 
neck blackish; tentacles subcylindhc, 
pointed, translucent in first quarter, changing 
sharply to dark gray or black; mantle skirt 
light gray. Palliai cavity elongate; mantle or- 
gan forming conspicuous pouch; kidney very 
elongate. 

Radula (Figs. 346-350) having formula 
[29 + (1 + 15) + 1 + (15 + 1) + 29] X 113. 
Central tooth base twice width of lateral teeth 
base, triangular, with conspicuous promi- 
nences on inner surfaces of arms; crown nar- 
rower and smaller than that of lateral teeth, 
with posterior edge straight or with weak me- 
dial depression; mesocone small, pointed; 
very weak ectocones sometimes present. 
Lateral teeth 14 to 17; crown broadly trian- 
gular, half total tooth length; mesocone 
sharp, pointed laterally; first lateral tooth with 
medial posterior part of crown elongate, with 
weak endocone; remaining lateral teeth with- 
out endocone, posterior edge of crown with 
medial prominence, medial posterior part of 
base flaring, cusp-shaped; no ectocone. 
Transitional tooth with weak ectocone. Mar- 
ginal teeth 24 to 32; base reduced, crown 
very elongate in first teeth, gradually becom- 
ing smaller; mesocone strong, sharp, gradu- 
ally becoming rounded at tip. 

Digestive system as in Melampus s. s.; 
stomach (Fig. 351) as in subfamily. 

Reproductive system (Fig. 352) with 
ovotestis leaf-like, round, dark brown; albu- 
men gland spiral; prevaginal caecum con- 
spicuous; bursa duct connecting with vagina 
opposite exit of posterior vas deferens; bursa 
large, oval-elongate; vagina thin, long, about 
same size as posterior vas deferens; penis 
thin, long; anterior vas deferens about 65% 
of penis length; penial retractor attaching to- 
gether with columellar muscle. 

Nervous system (Fig. 353) having cere- 
bral commissure narrower than width of ce- 
rebral ganglion; left parietovisceral connec- 
tive twice the length of right one. 



292 



MARTINS 




FIGS. 334-345. 



WESTERN ATLANTIC ELLOBIIDAE 



293 




FIGS. 346-349. Melampus (D.) monile. radular teeth, Shelly Bay, Bermuda, si 11.2 mm. (346) Central and 
lateral teeth. (347) Transitional and marginal teeth. (348,349) Marginal teeth. Scale 50 цт. 



Remarks: Bruguière (1789) clearly stated 
that his Bulimus monile was from the West 
Indies, but the works he cited refer to both 
the West hdies (Lister, 1 770: pi. 834, figs. 60, 
61, Barbados) and East Indies (Martini, 1773: 
2, p. 126, pi. 43, fig. 444, East Indies). It was 
probably this discrepancy that led Dillwyn 
(1817) to suggest that Bruguière's Bulimus 
monile was only a variety of Voluta flava 
Gmelin, 1 791 . This, in turn, led to the general 
confusion of Bulimus monile with Voluta flava 
and the general use of the latter nanne for the 
West Indian species. Gmelin (1791: 3431), 
however, under Voluta flava referred only to 
figure 444 of Martini (1773), which definitely 
represents an East Indian species. 
Another explanation for the confusion of 



the two species, besides common reference 
to Martini's fig. 444, might reside in the vari- 
able color pattern of the West Indian species. 
The juveniles of Melampus (D.) monile, like 
those of Melampus flavus, are often golden or 
golden brown, as seen in С В. Adams' 
Melampus coronatus [= Melampus (D.) mo- 
nile, juvenile]. Bruguière (1789) in the original 
description stated that his specimens of 
Melampus (D.) monile were not fully grown, 
because they lacked the inner dentition of the 
outer lip, a feature reported by Lister (1770) 
and Martini (1773). This might explain his 
statement about the "very light yellow" color. 
Binney (1859), using the name Melampus 
flavus Gmelin, 1 791 , for the West Indian spe- 
cies, listed Melampus torosa Mörch and 



FIGS. 334-345. Melampus (D.) monile (Bruguière). (334) Specimen perhaps figured by Binney (1859:167, 
fig. I\A) (USNM 39827), si 12.8 mm. (335) Shelly Bay, Bermuda, si 14.4 mm. (336) M. flavus purpureas Davis, 
lectotype (ANSP 86922), South Shore, Bermuda, si 10.0 mm. (337) M. flavus albus Davis, lectotype (ANSP 
86924), South Shore, Bermuda, si 8.6 mm. (338) San Juan, Puerto Rico, si 12.6 mm. (339) San Juan, Puerto 
Rico, si 12.5 mm. (340) San Juan, Puerto Rico, si 12.2 mm. (341) Juvenile, Maravén, Venezuela, si 1.67 mm. 
(342) M. coronatus С В. Adams, lectotype (MCZ 186029), Jamaica, si 3.0 mm. (343,344) Lateral and top 
views of spire and protoconch, Indian Key Fill, Florida. (345) Detail of spire and protoconch of specimen of 
Fig. 341. Scale 500 |.im. 



294 



MARTINS 



С 1L 2L 



17L Т 1М 2М 




11М 13М 18М 20М 26М 28М 




FIG. 350. Melampus (D.) monile, radula, Shelly Bay, 
Bermuda. Scale 10 цт. 





FIG. 352. Melampus (D.) monile, reproductive sys- 
tem, Clifton Pt., New Providence, Bahamas. Scale 
1 mm. 



prvc prg pig cplc qx cc cg bg 




cbc bc 



FIG. 351. Melampus (D.) monile, stomach, Ber- 
muda. Scale 1 mm. 



vg piprc pipe 



Melampus (D.) monile (Bruguière) as syn- 
onyms. Under Melampus torosa, Mörch 
(1852) cited figure 444 of Martini (1773), in- 
cluded Voluta flava Gmelin in the synonymy 
and mentioned the Antilles as the locality. It 
appears, then, that Mörch also confused 
Melampus flavus (Gmelin) with Melampus (D.) 
monile (Bruguière) and Mörch's name must 
be treated as a synonym of Melampus (D.) 
monile (Bruguière, 1789). 

Another name listed in Mörch's (1852) 



FIG. 353. Melampus (D.) monile, central nervous 
system, Clifton Pt., New Providence, Bahamas. 
Scale 1 mm. 



Yoldi Catalogue is Melampus fusca from the 
Antilles. In the synonymy he cited Martini 
(1773, pi. 43, fig. 445), Voluta minuta Gmelin, 
1791, which prompted Binney (1859) to in- 
clude Melampus fusca as a synonym of 
Melampus (M.) coffeus, and Voluta monile. 
Figure 445 of Martini, upon which Voluta 



I 



WESTERN ATLANTIC ELLOBIIDAE 



295 



minuta Gmelin was based, has already been 
shown to be unidentifiable [see the remarks 
for Melampus (M.) coffeus]. Thus, the only 
citation under Melampus fusca that can sup- 
port the name is Voluta monile, of which 
Melampus fusca Mörch must be considered 
a synonym. 

Dall & Simpson (1901) found it difficult to 
separate Melampus (D.) monile; erroneously 
listed as Melampus flavus, from Melampus 
(M.) coffeus, owing to similarities in shape 
and color. They noted that the apertural den- 
tition is the most reliable distinguishing char- 
acter. Bruguière (1789) for Melampus (D.) 
monile mentioned two teeth, a small, oblique 
columellar tooth and a smaller parietal tooth. 
Usually Melampus (M.) coffeus has one 
small, more or less oblique columellar tooth, 
and two readily visible parietal teeth, the pos- 
terior one the largest of the three. Some- 
times, however, the anterior parietal tooth is 
either very small or absent, hence the source 
of confusion. The twisted columellar tooth, 
the much smaller, hidden parietal tooth and 
the hairs (noticed by Shuttleworth in 1858) or 
pits on the shoulder of the body whorl and 
spire unmistakeably distinguish Melampus 
(D.) monile from Melampus (M.) coffeus, 
Melampus (M.) bidentatus and Melampus (D.) 
morrisoni. It differs from Melampus (D.) bul- 
laoides in its more conical shape, longer ap- 
erture and evenness of the riblets on the 
outer lip. The hairs and general aspect of the 
spire are similar to those of the latter species, 
but Melampus (D.) monile has a more regular, 
lower conical spire. 

Melampus (D.) monile was placed by Mor- 
rison (1951b) within the genus Pira H. & A. 
Adams. The reasons that I do not accept that 
decision are discussed in the remarks for De- 
tracia. Melampus (D.) monile is placed in the 
subgenus Detracia on the basis of shell, rad- 
ular and anatomical characters. The strong, 
twisted columellar tooth, the medial promi- 
nences on the base of the central radular 
tooth, the pouch-like mantle organ and the 
greater separation between foot and visceral 
mass are all typical characters of Detracia. 

Habitat: Melampus (D.) monile is unique 
among species of Detracia in its preference 
for living much closer to the high-tide mark 
than do any other species of the subgenus, 
which usually live farther inland. Melampus 
(D.) monile commonly lives under boulders 
above the high-tide mark along open rocky 
shores, together with Tralia (T.) ovula and Pe- 




FIG. 354. Melampus (D.) monile, geographic distri- 
bution. Open circle, locality from literature. 



dipes mirabilis. It can also occur in man- 
groves, but always near the high-tide mark. 

Range: Bermuda; Florida; West Indies, Cen- 
tral America to Guanabara Bay, Brazil (Rios, 
1975) (Fig. 354). 

Specimens Examined: FLORIDA: Indian 
River (MCZ 201670); Miami (ANSP 47603, 
294316; USNM 492589); Coconut Grove 
(MCZ 201093, 291380, 294258); Bhckell 
Hammock, Biscayne Bay (MCZ 291382); 6 
km S of Tavernier, Key Largo (MCZ 291385); 
Tavernier Key (USNM 492549a); Plantation 
Key (MCZ 294255); S of Ocean Drive, Plan- 
tation Key (A.M.); Tea Table Key (MCZ 
291009); Indian Key Fill, N of Indian Channel 
(A.M.); Long Key (MCZ 291 01 0; A.M.); Grassy 
Key (A.M.); Crawl Key (MCZ 294256; A.M.); 
Knight Key (A.M.); West Summerland Key 
(MCZ 291388; A.M.); Big Torch Key (ANSP 
189590); Key West (ANSP 56804; 174363; 
USNM 36062a, 596785); Boca Grande, Gas- 
parilla Island (ANSP 142273). TEXAS: Port 
Maria (USNM 711207). BERMUDA (ANSP 
56790, 85587; MCZ 24155, 24249, 24250; 
USNM 11421a, 94432b, 173648, 173649, 
173650, 228688): Fairyland (ANSP 99082); N 
of Shelly Bay Beach (A.M.); Coney Island 



296 



MARTINS 



(A.M.); Ferry Reach Park (R.B.); N end of 
Long Bird Bridge (A.M.); St. George's Island 
(USNM 621572); Castle Harbor (ANSP 
143319); Hungry Bay (USNM 171939, 
492555; A.M.); Agar's Island, Hungry Bay 
(MCZ 48124, 106521; A.M.); South Shore 
(ANSP 86922, 86924; MCZ 53063, 53064; 
USNM 109560, 109561); Boat Bay (USNM 
621691); S end of Ely's Harbour (A.M.); W 
side of Somerset Bridge (A.M.); Mangrove 
Bay (A.M.). BAHAMA ISLANDS (ANSP 
56799; MCZ 9946; USNM 37607): GRAND 
BAHAMA ISLAND (ANSP 374527): Running 
Mon Canal (ANSP 369779); Eight Mile Rock 
(ANSP 1 73262; MCZ 1 1 671 2); Caravel Beach 
[John Jack Point], Freeport (ANSP 370226); 
Dead Mans Reef [Sandy Bevan's Cay] (ANSP 
371225); McLeans Town (ANSP 369067); 
GREATABACO ISLAND (MCZ 241 40; USNM 
492580): Hope Town Harbor (ANSP 299391); 
Little Harbor (USNM 180520); Witch Point 
(ANSP 299483, 359150); Matt Lowes Cay 
(ANSP 299248); Marsh Harbor (MCZ 
275572); BIMINI ISU\NDS: Alicetown, North 
Bimini (MCZ 144132); opposite Cat Tail 
Pond, South Bimini (ANSP 325784); AN- 
DROS ISIJ\ND (MCZ 66755, 71633): Mor- 
gan's Bluff (A.M.); Mastic Point (USNM 
359884); South Mastic Point (A.M.); First is- 
land off Mintie Bar, SE end of South Bight 
(USNM 271785b); Mangrove Cay (USNM 
269968c); Lisbon Point, Mangrove Cay 
(USNM 269599a); Bastion Point, Mangrove 
Cay (USNM 269260); Long Bay Key (USNM 
269304); PARADISE ISLAND: (A.M.); NEW 
PROVIDENCE ISLAND (USNM 603913): Nas- 
sau (USNM 160765a); Culbert Point, 10 km 
ESE of Nassau (MCZ 107793); Bar Point 
(A.M.); Delaport Point (A.M.); W of Rock Point 
(A.M.); Clifton Point (A.M.); Clifton Pier (A.M.); 
shore off Millars Road (A.M.); Malcolm Creek 
(A.M.); Coral Harbor (USNM 679136); ROYAL 
ISLAND (USNM 468115a); CAT ISLAND: 
Arthurstown (MCZ 1 07833); 6 km E of Arthur- 
stown (MCZ 107825); RUM CAY (MCZ 
87849); LONG ISLAND: 3 km NE of O'Neill's 
(ANSP 173265; MCZ 113102); Simms (MCZ 
294259); Clarencetown (MCZ 113339); 
GREAT INAGUA: Matthewstown (MCZ 
291384). TURK'S & CAICOS: TURK'S IS- 
LAND (MCZ 201098; USNM 492474, 
509960). CUBA (ANSP 56801 , 56802; USNM 
492478): Jaimanitas (MCZ 294198); Habana 
(ANSP 93653); Cayo Birricu, N of Habana 
(ANSP 362824); Cojimar (ANSP 45089; MCZ 
131921, 131955); Matanzas (ANSP 87896; 
MCZ 294192); La Playa (MCZ 92045, 



131950, 189818, 294260); Versalles (MCZ 
291381); Cayo Cristo (MCZ 291389); Vara- 
dero (ANSP 110604; MCZ 201677; USNM 
598261); Cayo Galindo, Cárdenas Bay 
(ANSP 157578); Cayo Frances (MCZ 42106, 
131951); Siboney (USNM 533912); Agua- 
dora, Santiago (USNM 391879); Guantán- 
amo (ANSP 313059); Cabo Cruz (MCZ 
87887); Rancho Alma, Cienfuegos (MCZ 
291386). JAMAICA (ANSP 56803; MCZ 
186029, 201094, 294254, 294257; USNM 
6385, 94744, 492475, 492477, 492480): 
Montego Bay (USNM 441488); Falmouth 
(ANSP 397268); Robin's Bay (USNM 442026, 
442092); Jack's Bay (USNM 441926); Buff 
Bay (USNM 441196); Port Antonio (USNM 
440855); Priestmans River (USNM 492479); 
Manchioneal (R.B.); Rock Fort (USNM 
374242); Kingston (USNM 374270, 442730); 
Harbor Head, Kingston (USNM 375579); Pal- 
isadoes (USNM 442466); Runaway Bay 
(USNM 202658); Little River (USNM 128046). 
HAITI: Gonave Island (492531a); île-à-Vache, 
Soulette Bay (USNM 439191a); Port Salut 
(ANSP 226701; MCZ 183912); Les Cayes 
(USNM 439742); Baie Anglaise, near Aquin 
(USNM 439548a); Saltrou (USNM 439342, 
442819); Bizoton (USNM 439832a). DOMIN- 
ICAN REPUBLIC: Monte Cristi (MCZ 57591, 
57750, 291383); Puerto Plata (MCZ 291379, 
291387); Santa Bárbara de Samaná (ANSP 
1 73263; MCZ 57757); Cayo Chico, E of Santa 
Bárbara de Samaná (MCZ 57776); Cayo de 
Tamise (MCZ 57812); Isla La Matica, Playa 
Boca Chica, E of Santo Domingo (R.B.). PU- 
ERTO RICO: E of San Juan (USNM 683107); 
Puerta de Tierra, San Juan (A.M.); Punta 
Cerro Gordo (USNM 683012); Punta Agu- 
jereada (MCZ 233338); Arecibo (MCZ 
291391); Punta Arenas, N of Joyuda (A.M.); 
Lighthouse, Cabo Rojo (MCZ 294194; 
Ensenada Honda, Culebra Island (USNM 
161161). VIRGIN ISLANDS: ST. THOMAS 
(ANSP 56789; MCZ 294196; USNM 256035) 
ST. CROIX (ANSP 56788; USNM 621396) 
LESSER ANTILLES: ANTIGUA (MCZ 7151 1) 
off Falmouth (USNM 502116); North Bay 
Guana Island (MCZ 88870; ANSP 351799) 
GUADELOUPE (MCZ 294197; USNM 
492481): Anse-Dumont, Gosier (USNM 
758065); ST. VINCENT: (USNM 492473); Villa 
(USNM 487000); BARBADOS: (ANSP 56797; 
MCZ 291390; USNM 502108, 502109); 
Bridgetown (USNM 502115); Pelican Island 
(USNM 502110, 502112); Needham Point 
(USNM 502113); off Telegraph Station 
(USNM 502114); Maxwell's Coast (USNM 



WESTERN ATLANTIC ELLOBIIDAE 



297 



603784); San Blas (ANSP 56796); GRENADA: 
Prickly Bay (ANSP 297189); off Hardman Bay 
(ANSP 296483); TRINIDAD (MCZ 294193). 
CARIBBEAN ISLANDS: SWAN ISLAND (MCZ 
22938, 36611); CAYMAN ISLANDS: Cayman 
Brae (ANSP 296178; MCZ 294195); OLD 
PROVIDENCE ISU\ND: N of Ironwood Point 
(USNM 678831); ST. ANDREWS ISLAND 
(ANSP 154359; MCZ 88689); CURAÇAO: 
Port Marie & Daaibooi Baai (R.B.). MEXICO: 
Isla Mujeres, Yucatán (ANSP 284638); As- 
cension Bay, Quintana Roo (USNM 736381, 
736718). BELIZE: North Spot (ANSP 
281604); Belize (USNM 150281). HONDU- 
RAS: Utila Island (USNM 61185); Roatan Is- 
land (USNM 364701). COSTA RICA: Pórtete, 
Limón (USNM 702853, 706403). PANAMA: 
Limón Bay (USNM 732871, 734073); Fort 
Sherman, Devil's Beach, 9 km N of Colón 
(USNM 620529). COLOMBIA: Sabanilla 
(USNM 103467, 193611). VENEZUELA: Cayo 
Punta Brava, Parque Nacional de Morrocoy, 
Tucacas (A.M.); El Palito (A.M.); Borburata 
(USNM 784776); Maravén, Borburata, E of 
Puerto Cabello (A.M.). 

Melampus (Detracia) morrisoni 
new name 

Figs. 355-376 

Detracia clarki Morrison, 1951a: 18, figs. 2, 6 
[Key West, Florida; holotype USNM 
594588 (Fig. 355)]; Morrison, 1951b: 9; 
Morrison, 1958: 118-124 [habitat]; Ab- 
bott, 1974: 332; Emerson & Jacobson, 
1976: 191, pi. 26, fig. 24 [dubious illus- 
tration]; Vokes & Vokes, 1983: 60, pi. 22, 
fig. 16. Non Melampus clarki i White, 
1895. 

Description: Shell (Figs. 355-367) to 17.7 
mm long, ovate-conic to subcylindric, solid, 
shiny; uniformly white to dark brown or with 
as many as five spiral brown bands or with 
irregular yellowish axial markings on body 
whorl. Spire short to moderately high, with as 
many as 13.25 spirally grooved or pitted 
whorls. Body whorl about 80% of total 
length, with incised spiral lines on shoulder. 
Umbilical excavation sometimes present. 
Aperture about 90% of body whorl length, 
very narrow; inner lip with very strong, ob- 
lique, upcurved columellar tooth; posterior 
parietal tooth strong, sometimes upcurved, 
anterior parietal tooth sometimes fused with 
posterior one; outer lip with as many as 18 
uneven internal riblets, not reaching edge; 



when numerous, not more than five riblets 
extend inside aperture. Partition of inner 
whorls occupying about 75% of body whorl 
(Fig. 361). Protoconch smooth, translucent, 
brownish (Figs. 365-367). 

Animal whitish, mottled with irregular 
brown spots, or uniformly black becoming 
lighter toward yellowish gray foot; tentacles 
subcylindric, pointed, discolored at base, 
dark toward tip; mantle skirt yellowish gray. 

Radula (Figs. 368-372) having formula [29 
+ (1 + 20) + 1 + (20 + 1) + 29] X 110. Base of 
central tooth wider than that of lateral teeth, 
triangular, weakly constricted laterally, with 
small medial prominence on inner surface of 
arms; crown length half of lateral teeth; me- 
socone small, sharp; ectocones very small or 
lacking. Lateral teeth 15 to 28; crown strong, 
cuneiform, half total length of tooth; meso- 
cone sharp, pointed laterally; no distinct ec- 
tocone or endocone. Transitional tooth with 
elongate crown, with either weak ectocone or 
serrated edge at site of ectocone. Marginal 
teeth 23 to 42, with reduced base; crown 
high; mesocone very strong, sharp, rapidly 
becoming round at tip; first marginal tooth 
with ectocone, becoming bicuspid on sec- 
ond marginal tooth and tricuspid on third; 
fourth cusp appears on seventh or eighth 
marginal tooth; endocone visible on fourth 
marginal tooth; outer edge of base gradually 
shortening posteriorly, fusing with crown and 
assuming shape of denticle stronger than ec- 
tocone cusps. 

Digestive system as in Melampus s.S.; 
stomach (Fig. 373) as in subfamily. 

Reproductive system (Fig. 374) with 
ovotestis leaf-like, circular, dark brown; albu- 
men gland spiral, conical; prevaginal caecum 
very conspicuous; bursa duct connecting 
with vagina just before exit of posterior vas 
deferens; bursa elongate; vagina thin, with 
length corresponding to nearly one and one- 
fifth the length of body whorl; penis thin, 
slightly longer than associated vas deferens. 

Nervous system (Fig. 375) with cerebral 
commissure about as long as width of cere- 
bral ganglion; left parietovisceral connective 
slightly larger than to twice size of right one. 

Remarks: Morrison (1951a) described this 
species as Detracia clarki. The anatomy of 
Detracia, however, does not justify generic 
rank and this taxon is here considered a sub- 
genus of Melampus (see the remarks for 
Melampus s. /.). The name Melampus clarki 
was used by White (1895) for a fossil shell, 



298 



MARTINS 




FIGS. 355-367. 



WESTERN ATLANTIC ELLOBIIDAE 



299 




FIGS. 368-371. Melampus (D.) morrisoni, radular teeth, Plantation Key, Florida. (368) Central and lateral 
teeth, si 12.9 mnn. (369) Marginal teeth, si 12.9 mm. (370) Central and lateral teeth of juvenile, si 1.8 mm. 
(371) Marginal teeth of juvenile, si 1.8 mm. Scale 50 |.im. 



later chosen as the type species of the genus 
Melampoides Yen, 1 951 . The inclusion of De- 
tracia as a subgenus of Melampus creates a 
case of secondary homonymy. A new name 
is necessary and I hereby rename the species 
Melampus (Detracia) morrisoni, in honor of J. 
P. E. Morrison and in appreciation for his 
work on the Ellobiidae. 

Melampus (D.) morrisoni is unusual among 
members of this subgenus in having a con- 
spicuous parietal tooth. In the other mem- 
bers of the group this tooth is not readily 
visible owing to its being deep within the ap- 
erture. The strong columellar tooth, the 
greater length of the palliai gonoducts, the 
pouch-like mantle organ and the medial 
nodes on the base of the central tooth of the 
radula justify removing this species from 



С IL 2L 19L 1Т 2Т IM 2М 




6М 7М 13М 14М 17М 18М 23М 25М 




FIG. 372. Melampus (D.) morrisoni, radula. Planta- 
tion Key, Florida. Scale 10 цт. 



FIGS. 355-367. Melampus (D.) morrisoni, new name. (355) Detracia clarki Morrison, holotype (USNM 
594588), Key West, Florida, si 12.5 mm. (356) Grassy Key, Florida, si 13.6 mm. (357) Grassy Key, Florida, 
si 14.0 mm. (358) Grassy Key, Florida, si 17.7 mm. (359) Grassy Key, Florida, si 15.7 mm. (360) Grassy Key, 
Flonda, 14.2 mm. (361) Plantation Key, Florida, si 12.8 mm. (362) Key Largo, Florida, si 12.7 mm. (363) 
Juvenile, Long Key, Florida, si 2.15 mm. (364) Millars Sound, New Providence, Bahamas, si 13.8 mm. 
(365-367) Lateral and too views of spire and protoconch. Long Key, Florida. Scale 500 |jm. 



300 



MARTINS 




FIG. 373. Melampus (D.) morrisoni, stomach, Flor- 
ida. Scale 1 mm. 




FIG. 374. Melampus (D.) morrisoni, reproductive 
system, Grassy Key, Florida. Scale 1 mm. 



Melampus s. s. and placing it in Detracia, 
however. 

Melampus (D.) morrisoni can be confused 
with Melampus (M.) bidentatus because they 
converge in shape and color and are similar 



in their variability. In its typical form, Melam- 
pus (D.) morrisoni is readily distinguished by 
its very narrow shell aperture, well-devel- 
oped, upcurved columellar tooth, numerous 
whorls and its more globose shape. Some 
populations from inner lagoons, in which they 
occur with Melampus (M.) bidentatus, show 
gradation to an average-sized columellar 
tooth and a common ovoid shape (Fig. 364). 
In such cases anatomical studies are helpful. 
The combination of a greater value of vagina 
length/body whorl length and the slightly 
higher number of whorls/shell length charac- 
terizes Melampus (D.) morrisoni. The latter 
species also can resemble the morphs of 
Melampus (M.) coffeus that have a less pro- 
nounced carina on the shoulder of the body 
whorl. The strong, curved columellar tooth, 
the presence of striae on the shoulder of the 
body whorl, the narrow aperture and the un- 
even outer lip riblets of Melampus (D.) morri- 
soni clearly separate this species from 
Melampus (M.) coffeus. 

As do other members of the genus, 
Melampus (D.) morrisoni undergoes a change 
in radular morphology with age (Figs. 370, 
371). The central tooth has weak but distinct 
ectocones. The first lateral tooth, deeply tri- 
cuspid in very young individuals, becomes 
bicuspid, then unicuspid, with serrated 
edges on the sites of the endocone or ecto- 
cone, or both. The transitional tooth develops 
an endocone, which remains through the 
marginal teeth. The marginal teeth have more 
ectocone cusps in the juvenile than in the 
adult. The radula of juveniles very strongly 
resembles in tooth count and morphology 
that of the adult Melampus (D.) floridanus 
(Figs. 324-327). This similarity suggests 
some degree of neoteny in radular develop- 
ment within the genus Melampus. 

Habitat: Melampus (D.) morrisoni lives in as- 
sociation with Melampus (M.) bidentatus and 
Melampus (D.) bullaoides. It prefers sheltered 
inland places in which the mangrove is thin 
and reached only by very high tides. Individ- 
uals aggregate under rocks and in old bur- 
rows of fiddler crabs. 

Range: South Florida [the St. Augustine 
record is dubious, according to Morrison 
(1951a)]; Bahama Islands south to Cuba and 
Yucatán, Mexico (Fig. 376). 

Specimens Examined: FLORIDA: St. Augus- 
tine (USNM 492529a); Grant (MCZ 291233); 
Miami (ANSP 189594, 294333; USNM 



WESTERN ATLANTIC ELLOBIIDAE 

prvc pg piprc pig pc cpc cc 



301 



cg ^ cbc 




vg prg pipe 



FIG. 375. Melampus (D.) morrisoni, central nervous system, Grassy Key, Florida. Scale 1 mm. 









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, ^ 


/^ 




■ 


"\^ 


-■4 
















""^^W^ 




4s 






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b~- 


^ 






^ 




j 








f 





FIG. 376. Melampus (D.) morrisoni, geographic dis- 
tribution. 

82844a); Brickell's Hammock, Miami (ANSP 
294334); Virginia Key (ANSP 189591; USNM 
82859a); Biscayne Bay (MCZ 291230); Flor- 



ida City (ANSP 294335); Middle Key, Barnes 
Sound (USNM 338339a); Pumpkin Key, Card 
Sound (USNM 355114); Key Largo (MCZ 
291232; USNM 603120); N of Tavernier 
Creek, Key Largo (A.M.); 6 km S of Tavernier 
(MCZ 291234); Tavernier Key (USNM 
492552a); S of Ocean Drive, Plantation Key 
(A.M.); Windley Key (USNM 603105); Indian 
Key (USNM 462894); Indian Key Fill, N of In- 
dian Key Channel (A.M.); Lower Matecumbe 
Key (USNM 492554, 700774); Long Key 
(A.M.); Grassy Key (MCZ 291236; A.M.); 
Crawl Key (MCZ 291042); Marathon, Key 
Vaca (ANSP 294336; MCZ 294264); Knight 
Key (A.M.); Bahia Honda Key (ANSP 189576; 
USNM 269777, 269980); Spanish Harbor Key 
(USNM 667407); Newfound Harbor (USNM 
272688, 338376); Little Pine Key (USNM 
681638); Big Pine Key (ANSP 189583; MCZ 
294270; USNM 104092a); end of Kohen 
Avenue, Big Pine Key (A.M.); Howe Key 
(USNM 681639); Big Torch Key (ANSP 
189579; A.M.); Ramrod Key (MCZ 291043, 
294263); Geiger's Key (ANSP 189582); Sug- 
arloaf Key (ANSP 189577; USNM 104094a); 
Porpoise Point, Big Coppit Key, 5 km N of 
Key West (MCZ 275573); Boca Chica Key 
(ANSP 189593; USNM 270329); Stock Island 
(ANSP 189581; USNM 594589); Key West 
(ANSP 180089, 189578; MCZ 291235; 



302 



MARTINS 



USNM 36062, 668245); Chokoloskee Key 
(ANSP 93430). BAHAMA ISLANDS: GRAND 
BAHAMA ISLAND (ANSP 374526): North 
Riding Point (ANSP 371 539); GREAT ABACO 
ISLAND: Witch Point (ANSP 359152; USNM 
594592); Angel Fish Point (MOZ 294265); 
NEW PROVIDENCE ISIJ\ND: Millars Sound 
by Bacardi Road (A.M). CUBA: Cape Cajón 
(USNM 492571); Cayo Perro (ANSP 189575; 
USNM 594590). Cayo Juan Garcia (MCZ 
291231); Cayo Maja, near Cayo Santa Maria 
(MCZ 294217). MEXICO: Isla Mujeres, Quin- 
tana Roo, Yucatán (R.B.). 

Genus Tralia Gray, 1840 

Tralia Gray, 1 840: 21 . Type species by mono- 
typy: Tralia pusilla (Gmelin, 1791) [= Vo- 
luta ovula (Bruguière, 1789)]. 

Tralica Gray. Reeve, 1877, pi. 1 [in synonymy 
of Auricula; error for Tralia]. 

Description: Shell thick, oval-elongate; aper- 
ture moderately long, widest part anterior to 
columellar tooth; inner lip with three white 
teeth, first parietal strongest; outer lip thick- 
ened, slightly reflected, with distinct anal 
groove. 

Animal white; tentacles flat dorso-ventrally. 
Internal edge of arms of central radular tooth 
with prominent medial nodes; first lateral 
tooth with conspicuous endocone; transition 
to marginal teeth marked. Salivary glands at- 
tached lateroventrally to esophagus; esoph- 
agus white. Ovotestis granular; mucous gland 
very convoluted, not clearly spiral; bursa duct 
connects at some distance from proximal end 
of vagina; penis very long, muscular. 

Remarks: The genus Tralia was created by 
Gray (1840) for the West Indian Tralia pusilla 
(Gmelin) [= Tralia ovula (Bruguière)] on the ba- 
sis of the peculiar, simple outer lip with its 
distinct anal groove. H. & A. Adams (1855b: 
244) separated Tralia Gray from Melampus 
Montfort on the basis of the incorrect obser- 
vation, "the foot was posteriorly acute, en- 
tire." The Adams brothers were confused, 
however, for they commented, "This group, 
which appears to have a simple, undivided 
tail, . . . perhaps, when the animals are better 
known, will be found to be merely a subge- 
nus of Melampus.'" 

H. & A. Adams recognized four subgenera 
of Tralia, Pira, Tifata, Signia and Persa. I have 
commented on Pira and Tifata under the re- 
marks for Detracia Gray. Signia, the third 



subgenus of Tralia introduced by H. & A. Ad- 
ams (1 855b), was later treated as a subgenus 
of Melampus by Thiele (1931) and Zilch 
(1959). The fourth subgenus, the Pacific 
Persa, was recognized by Thiele and Zilch as 
belonging to the genus Tralia; it is character- 
ized by the very short spire and by the con- 
vex, distinctly ribbed whorls. Another subge- 
nus also placed in Tralia was introduced by 
the Adams brothers in 1855 as Siona, a ge- 
nus of Cassidula, just prior to the publication 
of their Genera of Recent Mollusca. In this 
latter publication they changed the name to 
Sarnia without specifying the reason. Thiele 
(1931) recognized Siona as belonging to Tra- 
lia; Zilch (1959) noted that the name Siona 
was preoccupied and that Sarnia should be 
the correct name. The type of the subgenus, 
Tralia (Sarnia) frumentum (Petit, 1842), from 
South America, is an Eastern Pacific species 
conchologically very similar to the eastern 
North Atlantic Pseudomelampus exiguus 
(Lowe, 1832) [Pedipedinae] and to the genus 
Microtralia (Figs. 174-181). Keen (1971) con- 
sidered Pseudomelampus to be synonymous 
with Sarnia and placed it within the Ellobii- 
nae. According to Marincovich (1973) the 
radula of Tralia (Sarnia) frumentum is similar 
to that of Ellobium, and he considered Sarnia 
to belong in the Ellobiinae. It appears, then, 
that Sarnia cannot be considered a subgenus 
of Tralia. I have considered Sarnia, on the 
basis of the conchological resemblances 
with Pseudomelampus, to belong in the Pe- 
dipedinae (see the remarks under the Ellobi- 
idae). A study of the reproductive and ner- 
vous systems is needed to ascertain its 
phylogenetic position, however. 

Binney (1 865: 1 6, fig. 1 6) figured the animal 
of an alleged Tralia, but admitted in a foot- 
note that he did not know which species it 
represented. Simpson drew from nature a 
figure of an animal from Charleston, South 
Carolina, a locality that is not in the range of 
Tralia (T.) ovula. I concur with Dall (1885) that 
Simpson's drawing probably represents My- 
osotella myosotis (Draparnaud). 

The genus Tralia is readily distinguished 
from Melampus by its wide anterior aperture, 
its strong first parietal tooth and its thickened 
outer lip with a subposterior internal groove. 

The apertural dentition of Tralia is unusual 
for a member of the Melampinae and, after 
anatomical research is carried out, it is pos- 
sible that some Indo-Pacific species pres- 
ently put in this subgenus will be found to 
belong to other subfamilies. 



WESTERN ATLANTIC ELLOBIIDAE 



303 



Habitat: The only information available about 
the habitat of the genus refers to the West 
Indian Tralla (T.) ovula and, for this reason, 
comments on habitat will be made under that 
species. 

Range: Tralla is a tropical group, living 
mostly in the Indo-Pacific. It is represented in 
the West Indies by one species, Tralla (T.) 
ovula, which seems to have been introduced 
in West Africa. 

Subgenus Tralla s. s. 

Description: Shell to 16 mm long; spire mod- 
erately high, with pitted lines; body whorl 
smooth or weakly marked with punctate spi- 
ral lines. 

Remarks: see the remarks under Tralla s. I. 



Tralla (Tralla) ovula (Bruguière, 1789) 
Figs. 377-387, 389-400 

Bullmus ovulus Bruguière, 1789: 339 [Guade- 
loupe, West Indies; location of type un- 
known]; Cuvier, 1817: 414. 

Voluta pusllla Gmelin, 1 791 : 3436 [locality un- 
known, herein designated to be Guade- 
loupe, West Indies; location of type un- 
known]; Dillwyn, 1817: 507; Wood, 1825: 
91, pi. 19, fig. 20; Hanley, 1856: 98, pi. 
19, fig. 20. 

Voluta triplicata Donovan, 1802, pi. 138 [lo- 
cality unknown, herein designated to be 
Guadeloupe, West Indies; location of 
type unknown]; Montagu, 1808: 99; Dill- 
wyn, 1817: 507; Wood, 1825: 91, pi. 19, 
fig. 19; Hanley, 1856: 98, pi. 19, fig. 19. 

Auricula (Conovulus) ovula (Bruguière). Fér- 
ussac, 1821: 104; Rang, 1829: 173. 

Auricula nitens Lamarck, 1822: 141 [Guade- 
loupe, West Indies; type in the MHNG 
(Mermod, 1952)]; Menke, 1830: 36; 
Gould, 1833: 67; Jay, 1839: 59; Küster, 
1844: 18, pi. 2, figs. 11-13. 

Melampus ovulum Schweigger. Lowe, 1832: 
289. 

Pythia triplicata (Donovan). Beck, 1837: 104. 

Pythia ovulum (Bruguière). Beck, 1837: 104. 

Auricula ovula (Bruguière). Rotiez & Michaud, 
1838: 204, pi. 20, figs. 13, 14. 

Auricula pusilla (Gmelin). Deshayes. 1838: 
332. 

Auricula (Conovulus) pusillus Deshayes. An- 
ton, 1839: 48. 



Tralla pusilla Gray. Gray, 1840: 21. 

Auricula ovula Fèrussac. Orbigny, 1841: 186, 
pi. 13, figs. 1-3. 

Tralla pusilla (Gmelin). Gray, 1847a: 179; H. & 
A. Adams, 1855b: 244, pi. 82, fig. 8; Bin- 
ney, 1 865: 1 7, fig. 1 8; Tryon, 1 866: 9, pi. 
18, fig. 9; Dohrn, 1866: 133 [first record 
from Eastern Atlantic]; Dal!, 1885: 276, 
pi. 18, fig. 5; Dall, 1889: 92, pi. 47, fig. 5; 
Dall In Simpson, 1889: 69; Dall & Simp- 
son, 1901: 369, pi. 59, fig. 13; Odhner, 
1925: 5, pi. 1, fig. 8B, pi. 2, fig. 18 [radula 
and reproductive system figured]; Reile, 
1926: 88; 0. W. Johnson, 1934; 159; 
Coomans, 1958: 103, pi. 10; Franc, 
1968: 525. 

Melampus pusillus (Gmelin). G. B. Adams, 
1849: 42; C. B. Adams, 1851: 186; 
Pfeiffer, 1854b: 147: Pfeiffer, 1856a: 46 
[erroneously stated as also inhabiting 
Hawaii]; Binney, 1859: 168, pi. 75, fig. 
29; Binney, 1860: 4; Poey, 1866: 394; 
Jeffreys, 1869: 109; Pease, 1869: 61; 
Pfeiffer, 1876: 317; Arango y Molina, 
1880: 59; Crosse, 1890: 258. 

Melampus (Tralla) pusillus (Gmelin). H. & A. 
Adams, 1854: 10. 

Melampus nitens (Lamarck). Shuttleworth, 
1854b: 101; Shuttleworth, 1858: 73; 
Mörch, 1878: 5; Nevill, 1879: 219. 

Tralia pusilla Linnaeus. Fischer & Crosse, 
1880: 22. 

Tralia (Tralla) pusilla (Gmelin). Thiele, 1931: 
466. 

Tralla ovula (Bruguière). Morhson, 1951b: 9; 
Nowell-Usticke, 1959: 88; Coomans, 
1969: 82; Warmke & Abbott, 1961: 153, 
pi. 28, fig. m; Morris, 1973: 274, pi. 74, 
fig. 10; Abbott, 1974: 332, fig. 4095; 
Emerson & Jacobson, 1976: 193, pi. 26, 
fig. 29; Gibson-Smith & Gibson-Smith, 
1 982: 1 1 7; Vokes & Vokes, 1 983: 60, pl. 
22, flg. 17; Mahieu, 1984, 314 pp. 

Tralia (Tralla) ovula (Bruguière). Zilch, 1959: 
67, fig. 215. 

Tralia ovula sculpta Nowell-Usticke, 1959: 88 
[St. Croix-by-the-Sea, Cane Bay, St. 
Croix; lectotype herein selected AMNH 
220313 (Fig. 384); listed on page VI as 
Tralia ovulata sculpta]. 

Tralla cf. ovula (Bruguière). Gibson-Smith & 
Gibson-Smith, 1979: 22 [Cantaure For- 
mation, Venezuela (Miocene)]. 

Tralia venezuelana Gibson-Smith & Gibson- 
Smith, 1982, figs. 7-9 [Borburata, Falcon 
State, Venezuela; holotype USNM 
784719 (Fig. 377). 



304 



MARTINS 



Description: Shell (Figs. 377-387, 389-391) 
to 16 mm long, oval-elongate, solid, shiny, 
uniformely chestnut brown to dark purplish 
brown, sometimes with one or two paler 
bands on body whorl. Umbilicus present. 
Spire low to moderately high, with as many 
as nine flat whorls sculptured with four or five 
spiral rows of deep pits. Body whorl averag- 
ing 85% of shell length, oval-elongate, with 
striated, uncarinate shoulder; striations visi- 
ble over entire body whorl of most young, 
commonly only on anterior region in adults. 
Aperture averaging 85% length of body 
whorl, posteriorly angulate, widely rounded 
anteriorly, white to dark purple inside; inner 
tip with three evenly spaced, large white 
teeth; columellar tooth and posterior parietal 
tooth of same size, reversely oblique, col- 
umellar tooth inclined toward base of aper- 
ture; first parietal tooth strongest, perpendic- 
ular to columellar axis; excavation posterior 
to second parietal tooth, bordered outside by 
more or less conspicuous callus, continuing 
inwards, commonly with small irregularities, 
sometimes with prominent denticle; outer lip 
sharp in juveniles, thick and weakly reflected 
in gerontic individuals, weakly sinuous pos- 
teriorly and with thick callous denticle inside, 
opposite second parietal tooth; outer lip den- 
ticle ridge-like, continuing inside aperture, to- 
gether with second parietal tooth delimiting 
relatively wide canal. Inner partition of whorls 
occupying less than half of the body whorl 
(Fig. 379). Protoconch smooth, yellowish to 
brown, with nucleus visible (Figs. 389-391). 
Animal white; foot with transverse groove, 
whitish, with minute brown spots over bifid 
posterior end; tentacles dorsoventrally flat- 
tened, spatulate, with first quarter bulbous, 
white, abruptly changing to dark grey or 
black toward tip; seminal groove unpig- 
mented; mantle skirt with very small brown 
spots over light brown background. Kidney 



rectangular, elongate; mantle organ well de- 
veloped, not pouch-like. 

Radula (Figs. 392-396) having formula [38 + 
(1 + 15) + 1 + (15 + 1) + 38] X 115. Base of 
central tooth with conspicuous medial prom- 
inences on inner edge of arms; crown length 
about half of that of lateral teeth, broadly tri- 
angular anteriorly, elongate posteriorly; ecto- 
cones absent. Lateral teeth 13 to 19; crown 
broadly triangular; conspicuous endocone on 
first lateral tooth; posterior medial portion of 
base of remaining lateral teeth flaring at junc- 
ture with crown, simulating endocone; last lat- 
eral tooth sometimes with very weak ecto- 
cone. Transitional tooth with lateral portion of 
crown posteriorly elongate, with tricuspid ec- 
tocone; base almost straight. Marginal teeth 
35 to 43; crown very elongate and irregularly 
pointed posteriorly; mesocone sharp, long, 
becoming rounded, spatulate, almost as long 
as remaining denticles, but much stronger; 
first marginal tooth with conspicuous en- 
docone and a tricuspid ectocone; as many as 
nine ectocone cusps on last ten marginal 
teeth. 

Digestive system with salivary glands at- 
tached close together by fine thread on ven- 
tral side of white esophagus; posterior crop 
very dilated, forming pouch before entering 
stomach; stomach (Fig. 397) as in subfamily; 
digestive gland pale yellow to bright orange. 

Reproductive system (Fig. 398) having 
ovotestis dark brown with whitish spots, gran- 
ular; mucous gland and albumen gland inter- 
penetrating at base; spermoviduct cylindrical, 
very muscular; bursa duct connecting at a 
point about one-fourth of total length from 
proximal end of long, muscular vagina; pos- 
terior vas deferens about 80% of vagina 
length; penis long, very muscular, with pos- 
terior half sometimes wrapped in membra- 
nous sheath; anterior vas deferens of variable 
length. 



FIGS. 377-391. Tralla. (377) T. venezuelana Gibson-Smith & Gibson-Smith, holotype (USNM 784719), 
Borburata, Falcon State, Venezuela, si 12.7 mm. (378) T. (T.) ovula (Bruguière), El Palito, Venezuela, si 13.6 
mm. (379) T. (T.) ovula, El Palito, Venezuela, si 13.5 mm. (380) T. (T.) ovula. San Juan. Puerto Rico, si 12.8 
mm. (381) T. (T.) ovula, Rock Pt., New Providence, Bahamas, si 14.9 mm. (382) T. (T.) ovula, llhado Principe, 
Gulf of Guinea (MCZ 73375), si 9.0 mm. (383) "Voluta triplicata Donovan," West Indies (USNM 442093), 
from Turton's Cabinet, Jeffreys collection, si 14.8 mm. (384) T. ovula sculpta Nowell-Usticke, lectotype 
(AMNH 220313), St.-Croix-by-the-Sea, Cane Bay, St. Croix, si 12.0 mm. (385) T. (T.) ovula. Haiti (MCZ 
18392), si 10.4 mm. (386) T. (T.) ovula, Robin's Bay, Jamaica (USNM 712378), si 6.4 mm. (387) T. (T.) ovula. 
juvenile, Maravén, Venezuela, si 2.3 mm. (388) T. vetula Woodring, holotype (ANSP 12506), Bowden, 
Jamaica, si 5.5 mm. (389) T. (T.) ovula, lateral view of spire and protoconch, Tucacas, Venezuela. (390) T. 
(T.) ovula, lateral view of spire and protoconch. Rock Pt., New Providence, Bahamas. (391) T. (T.) ovula, top 
view of spire and protoconch, Haiti (USNM 439659). Scale 1 mm. 



WESTERN ATLANTIC ELLOBIIDAE 



305 




FIGS. 377-391. 




FIGS. 392-395. Tralla (T.) ovula, radular teeth. (392-394) El Palito, Venezuela, si 14.7 mm. (395) Central 
tooth and adjacent lateral teeth, with articulation between base of one tooth and crown of next tooth, Bar 
Pt., New Providence, Bahamas, si 14.1 mm. Scale 50 (.im. 



С IL 2L 16L IM 2М ЗМ 




ЮМ 11М 12М 20М 21М 22М 30М31М32М 




FIG. 396. Tralla (T.) ovula, radula, El Palito, Vene- 
zuela. Scale 10 |am. 

Nervous system (Fig. 399) with cerebral 
commissure as long as width of cerebral 
ganglion; left parietovisceral connective two 
to three times longer than right one; left 
parietal ganglion half size of right one; vis- 



cr 




- — --ca 



FIG. 397. Tralla (T.) ovula, stomach, Venezuela. 
Scale 1 mm. 



WESTERN ATLANTIC ELLOBIIDAE 



307 




FIG. 398. Tralia (T.) ovula, reproductive system. A, Clifton Pt., New Providence, Bahamas; B, Puerto Rico, 
si 13.8 mm; C, Tucacas, Venezuela, si 10.9 mm; D, El Palito, Venezuela, si 13.8 mm. Scale 1 mm. 



308 



MARTINS 



spc PC pg pipe 




FIG. 399. Tralia (T.) ovula, central nervous system, 
San Juan, Puerto Rico, sl 13.8 mm. Scale 1 mm. 



cera! ganglion as large as right parietal gan- 
glion. 

Remarks: The names Bulimus ovulus Bru- 
guière, 1789, and Voluta pusilla Gmelin, 
1791, were thought to have appeared in the 
same year (Dall, 1 885) and early authors were 
more inclined to use the latter. In fact Bru- 
guière's name antedates Gmelin's and it has 
now been accepted as the correct name by 
most authors. 

Gmelin's description, although mentioning 
the tridentate columella, is brief and omits the 
geographic origin of the specimen. The fact 
that both Gmelin and Bruguière referred to 
Martini (1773, fig. 446) indicates that these 
authors were describing the same species. 

Donovan (1802) introduced Voluta tripli- 
cata (Fig. 383) based on material of unknown 
origin, although Montagu later stated (1808) 
that the specimens were from Guernsey, En- 
gland. As in the case of Melampus (D.) bul- 
laoides (Montagu) and of its junior synonym 
Auricula multivolvis Jeffreys, Donovan's ma- 
terial might have reached England in the bal- 
last of ships coming from the West Indies. 
Auricula (Conovulus) triplicatus Anton (1839) 
should not be confused with Donovan's spe- 
cies. Anton referred to the highest (posterior) 
parietal tooth as the strongest, a character- 
istic of most Pedipedinae. Connolly (1915) 
considered Anton's species a junior synonym 
of Marinula pepita King, 1832. 

Bruguière (1789) and Dillwyn (1817) both 
mentioned Martini's (1773) reference to fine, 
axial striations on the shell; this can refer only 
to the very fine growth lines that are some- 
times visible. The shell can be sculptured 



with well-marked spiral striae, however (Figs. 
387, 389-391). It was on the basis of the spi- 
ral striations that Nowell-Usticke (1959: 88) 
described Tralia ovula sculpta in two words, 
"spire lined" (Fig. 384). Shuttleworth (1858) 
was the first to mention the five deeply pitted 
spiral lines on the early whorls, erroneously 
adding that they were "ciliated" in juveniles. 
Juveniles and some adults of Melampus (D.) 
monile, which at a first glance can be con- 
fused with Tralia (T.) ovula, have a crown of 
hairs on the spire (Fig. 341), but neither the 
adults nor the young of Tralia (T.) ovula have 
hairs. 

Gibson-Smith & Gibson-Smith (1982) de- 
scribed Tralia venezuelana from Borburata, 
Venezuela (Fig. 377), which they distin- 
guished from Tralia (T.) ovula on the basis of 
its pitted spire and the presence of a fourth 
denticle in the aperture. I have observed a 
pitted spire, more or less pronounced, on all 
well-preserved specimens and on all young 
shells of Tralia (T.) ovula. It is particularly 
marked in some thin-shelled, elongate, dwarf 
morphs from Cuba, Jamaica, Haiti and St. 
Croix. The fourth denticle, in the shallow pos- 
terior parietal excavation, also occurs in 
specimens from Cuba, Jamaica, Haiti, Puerto 
Rico and St. Croix. Specimens from the Ba- 
hamas have an irregular surface on the pos- 
terior portion of the inner lip, but no distinct 
denticle. The fourth denticle seems to be a 
variable character, not associated with differ- 
ences in radula, anatomy, or shell. Presence 
of extra parietal teeth has been reported in 
the Pacific Melampus fasciatus, Melampus 
luteus and Melampus nucleolus and it is not 
considered a reliable taxonomic character for 
those species (Jickeli, 1872). Extra denticles 
also occur in Melampus (M.) coffeus and 
Melampus (M.) bidentatus (Martins, personal 
observation). I therefore have placed Tralia 
venezuelana Gibson-Smith & Gibson-Smith 
in the synonymy of Tralia (T.) ovula. 

In some Venezuelan specimens the poste- 
rior half of the very muscular penis was 
folded and wrapped in a membranous sheath 
(Fig. 398D). Such specimens also had an un- 
usually muscular spermoviduct and a shorter 
anterior vas deferens. Except for larger size 
(average 14 vs. 12 mm) no other shell and 
radular characters were associated with the 
phenomena. They were not associated with 
the presence of a fourth denticle on the ap- 
erture. It is possible that such phenomena 
are anomalies of gerontic specimens of that 
population. 



WESTERN ATLANTIC ELLOBIIDAE 



309 



There are two reports of fossil West Indian 
Tralia. Woodring (1928) described Tralia (T.) 
vetula from the Pliocene Bowden Formation 
of Jamaica (Fig. 388). After examining several 
lots of Recent material from Jamaica, I com- 
pared Woodring's example with the thinner- 
shelled, slender, dwarf specimens of Tralia 
referred to above; I found that these recent 
specimens show all gradations of thickness. 
Tralia (T.) vetula is considered a distinct spe- 
cies on the basis of the less pronounced den- 
tition of the inner lip, however. Gibson-Smith 
& Gibson-Smith (1979) reported a Tralia ? 
ovula from the Early Miocene Cantaure For- 
mation of Paraguaná, Venezuela, and also 
from the Late Pliocene Mare Formation of 
Cabo Blanco, Venezuela (Gibson-Smith & 
Gibson-Smith, 1982). In the latter publication 
the Gibson-Smiths identified those speci- 
mens with their Tralia venezuelana, which I 
consider synonymous with Tralia (T.) ovula. 

Habitat: Tralia (T.) ovula lives along the high- 
tide mark. The animals prefer piles of boul- 
ders on open rocky shores, but they also live 
in the less-protected mangroves. 









\ 












■ 


C*"^ 


\ \ • 








....У1^ 






\^ 








^ 


"^^^ 


-Y^*--^ 


^ 






— - 


\ 




i^- 






I 


J 1 1 



FIG. 400. Tralia (T.) ovula, geographic distribution. 



Range: Bermuda; Florida Keys; West Indies 
to Trinidad; Central America to Venezuela; 
llha do Principe, Gulf of Guinea, Africa (Fig. 
400). 

Specimens Examined: FLORIDA (USNM 
37597, 39873): Tavernier Key (USNM 
492519); Lower Matecumbe Key (USNM 
492595); Long Key (A.M.). BERMUDA (MCZ 
304151; USNM 6531, 94434). BAHAMA IS- 
LANDS (USNM 492465): GRAND BAHAMA 
ISU\ND (ANSP 173482, 375528): Eight Mile 
Rock (MCZ 294268); GREAT ABACO IS- 
LAND: Little Harbor (USNM 180486); AN- 
DROS ISLAND (MCZ 58507, 66744, 66756); 
NEW PROVIDENCE ISLAND: Nassau (USNM 
534924); Rock Point (A.M.); Clifton Point 
(A.M.); RUM CAY (MCZ 304157); LONG IS- 
LAND (ANSP 173483): 3 km NE of O'Neill's 
(MCZ 304152); GREAT INAGUA ISLAND: 
Matthewstown (MCZ 3041 53). TURK'S & CA- 
ICOS: TURK'S ISLAND (MCZ 304150; USNM 
492469, 509960a). CUBA (ANSP 56807; 
USNM 10965, 492472): Habana (MCZ 
294794); Cayo Birricu (ANSP 362825); Jai- 
manitas (MCZ 294199); Matanzas (ANSP 
167243; MCZ 304168); La Playa (MCZ 
304159, 304165); Versalles (MCZ 304154); 
Varadero (MCZ 304164); Caibahén (MCZ 



304163, 304175); Cayo Francés (MCZ 
294200); Siboney (USNM 533913); Punta de 
Piedras (MCZ 304166); Bahia de Santiago 
(MCZ 304161); Cabo Cruz (MCZ 304156). 
JAMAICA (ANSP 66964; MCZ 294269, 
304158, 304167, 304169, 304174; USNM 
49744a, 94745, 492467, 492471, 492593): 
Montego Bay (ANSP 359145); Robin's Bay 
(USNM 442092a, 442093); Jack's Bay 
(USNM 441834); Port Maria (USNM 711209); 
Buff Bay (USNM 441195); Stoney Cove 
(USNM 440762); Port Antonio (ANSP 62022; 
USNM 712147); Priestman's River (USNM 
492468); Manchioneal Bay (ANSP 61883; 
MCZ 9950; USNM 127359; R.B.); Port Royal 
(USNM 395452a, 442419a); Runaway Bay 
(USNM 202657); Little River (USNM 128047, 
492463). HAITI: Yuma River (ANSP 60950); 
St. Louis (USNM 439390); St. Marc (USNM 
492470); Port Salut (ANSP 226694; MCZ 
183922; USNM 440024); île-à-Vache (USNM 
401874, 401875, 439169); Les Cayes (USNM 
439746); Torbeck (USNM 402261, 439659); 
Aquin (USNM 403256a, 440170a); Baie Ang- 
laise, near Aquin (USNM 439548); between 
Vieux Bourg and Baïe des Flamands (USNM 
403425); N of Metesignix (USNM 404149); 
Saltrou (ANSP 387078; USNM 439342a, 
442813); Bizoton (USNM 439828a). DOMIN- 



310 



MARTINS 



ICAN REPUBLIC (MCZ 304172; USNM 
151297): Santo Domingo (ANSP 62910); 
Monte Cristi (MCZ 304162); Samaná (MCZ 
281639). PUERTO RICO: Puerta de Tierra, 
San Juan (A.M.); Rifle Range Beach, Punta 
Agurejeada (MCZ 233299); Arecibo (MCZ 
304160); Cabo Rojo Lighthouse (MCZ 
294202); Ensenada Honda, Culebra Island 
(USNM 169886). VIRGIN ISLANDS: ST. 
CROIX (ANSP 56806; MCZ 200448, 304155; 
USNM 621395): Prosperity Beach (MCZ 
304173); St. Croix-by-the-Sea, Cane Bay 
(AMNH 192356, 220313; ANSP 231952); ST. 
THOMAS (ANSP 56805, 359147; USNM 
250034, 530175); Sapphire Beach (ANSP 
306673); Water Bay (ANSP 56808); ST. 
JOHN'S (MCZ 304171); GUANA ISLAND 
(MCZ 294203): North Bay (ANSP 351790). 
LESSER ANTILLES: ANGUILLA BANKS (MCZ 
294201); ANTIGUA (ANSP 109155; USNM 
215048): off Falmouth (USNM 502098); 
GUADELOUPE (USNM 492466, 492518): 
Anse-Dumont, Gosier (USNM 758066); BAR- 
BADOS: (MCZ 304170, 304177, 304178; 
USNM 502104, 502105); Bridgetown (USNM 
502102); Needham Point (USNM 502101); 
Maxwell's Coast (USNM 603783); Pelican Is- 
land (USNM 502100); GRENADA: Prickly Bay 
(ANSP 297184); TRINIDAD: South Coast 
(ANSP 363992). CARIBBEAN ISU\NDS: 
SWAN ISLAND (MCZ 36612, 294267); CAY- 
MAN ISLANDS: Little Cayman (MCZ 294204); 
ST. ANDREWS ISLAND (ANSP 159360); CU- 
RAÇAO: Port Marie and Daaibooi Baai (R.B.). 
MEXICO: Ascension Bay, Ouintana Roo 
(USNM 736380). BELIZE: Belize (USNM 
151050). HONDURAS: Roatan Island (USNM 
364701a). COSTA RICA: Pórtete, Limón 
(USNM 702826, 706404). PANAMA: Fort 
Sherman, Devil's Beach (USNM 620530); 
Toro Point, Fort Sherman (USNM 732868, 
734071). COLOMBIA: Sabanilla (USNM 
193612). VENEZUELA: Cayo Punta Brava, 
Parque Nacional de Morrocoy, Tucacas 
(A.M.); El Palito (A.M.); Borburata (USNM 
784719, 784772); Maravén, Borburata (A.M.). 
EASTERN ATLANTIC: llha do Príncipe, Gulf of 
Guinea (MCZ 73375). 

CONCLUSIONS 

Phylogeny and Classification 

Gastropods have long been divided into 
prosobranchs, opisthobranchs and pulmo- 
nates. Ihering's (1876, 1877) anatomical re- 
search led him to conclude that the Gas- 



tropoda were polyphyletic. He derived the 
prosobranchs from the annelids, and the 
opisthobranchs and the pulmonates from 
the platyhelminths. Ihering's view has not 
been accepted and there is consensus that 
the gastropods are in fact monophyletic. A 
difference of opinion arises, however, about 
the way in which the generally more ad- 
vanced euthyneurans (opisthobranchs and 
pulmonates) are related to the more primitive 
streptoneurans (prosobranchs). Pelseneer 
(1894a) and Hubendick (1945) thought that 
the euthyneurans arose from the archaeo- 
gastropods. Pelseneer based his decision 
upon the similarities of the rhipidoglossan 
radula of the trochids with that of the ceph- 
alaspideans and basommatophorans. Mor- 
ton (1955c) slightly modified this view by 
proposing a pre-archaeogastropod as the 
ancestor of the archaeogastropods and eu- 
thyneurans. A different view was held by 
Fretter (1946, 1975), Boettger (1954) and 
Gosliner (1981), who considered the meso- 
gastropod stock as the ancestor of the eu- 
thyneurans. For the first two authors this 
origin would be located near the Rissoacea, 
on the basis of the size and habitat of the 
Recent species of that superfamily, which 
live in marine, estuarine, freshwater and ter- 
restrial habitats. Their small size could ex- 
plain the loss of the ctenidium, and the inva- 
sion of the terrestrial habitat would favor the 
secondary development of an air-breathing 
palliai cavity. In addition, the mesogastropod 
lineage explains the absence of the right kid- 
ney throughout the Euthyneura and the sim- 
ilarity of the reproductive tract with that of a 
female mesogastropod (Fretter, 1975). Gos- 
liner (1981), however, on the basis of the re- 
productive system, together with the fossil 
record, considered the Littorinacea as the 
stock that produced the euthyneurans. 

More recently emphasis has been put on 
the Pyramidelloidea Gray, 1840, a superfam- 
ily of mostly small streptoneurans assembled 
within the suborder Allogastropoda Haszpru- 
nar, 1985. Separation of this superfamily 
from the Opisthobranchia has favored the hy- 
pothesis of a common ancestry for the Pyra- 
midelloidea and euthyneurans (Haszprunar, 
1985, 1988; Salvini-Plawén & Haszprunar, 
1987). 

Traditionally the ellobiids have been con- 
sidered the living representatives of the prim- 
itive pulmonates and simultaneously they 
have been associated with the primitive 
opisthobranchs. Mörch (1865: 11) was the 



WESTERN ATLANTIC ELLOBIIDAE 



311 



first to recognize the affinities of pulmonates 
and opisthobranclns when, on the basis of 
their hermaphroditism, he included both 
groups within his subclass Androgyna. 
Pelseneer (1894a) broadened that relation- 
ship by also calling attention to their detorted 
(euthyneurous) nervous system. This euthy- 
neurous condition led some authors to con- 
sider both groups members of the subclass 
Euthyneura Spengler, 1881 (Boettger, 1954; 
Taylor & Sohl, 1962; Burch, 1962; Haszpru- 
nar, 1985). Others, while recognizing the 
close similarities between the two groups, 
still prefer the traditional terminology, consid- 
ering the Pulmonata and the Opisthobran- 
chia as separate subclasses (Morton, 1955c; 
Fretter & Graham, 1962; Robertson, 1973; 
Fretter, 1975; Hubendick, 1978; Salvini-Pla- 
wén, 1980). 

Pelseneer (1893, 1894a), Thiele (1935) and 
Boettger (1954) derived the pulmonates from 
the cephalaspidean Acteon and considered 
the ellobiids to be the link between the two 
groups. Pelseneer found support for his de- 
cision in the earlier fossil record of the 
acteonids and on the similarities of the shell 
apertures of the acteonids and ellobiids. 
Morton (1955c) suggested that these con- 
chological characters might be adaptive only 
and, as such, their taxonomic value is not 
significant. As Harry (1951) pointed out, the 
heterostrophy common to the ellobiids and 
the opisthobranchs constitutes a much 
stronger taxonomic character. More com- 
mon is the opinion that the opisthobranchs 
and pulmonates arose from the same proso- 
branch stock, not one from the other (Mor- 
ton, 1955c; Fretter, 1975; Gosliner, 1981). 

Within the pulmonates, the relationship 
between the basommatophorans and the 
stylommatophorans also has been the object 
of several hypotheses. Apart from the direct 
line"opisthobranch-ellobiid(basommatopho- 
ran)-stylommatophoran" scheme advocated 
by Pelseneer (1893, 1894a), Hedley (1917) 
and Boettger (1954), the more commonly 
held opinion is that the basommatophorans 
are too diverse to be considered collectively 
as ancestors to the stylommatophorans. 
Burch (1962), based on the number of chro- 
mosomes, proposed that a hypothetical pre- 
basommatophoran (called Ur-Basommato- 
phora) with opisthobranchiate ancestry might 
have given rise to Morton's (1955c) Archae- 
opulmonata and Branchiopulmonata. The 
first group includes the Ellobiidae, Amphibol- 
idae and Siphonahidae, commonly consid- 



ered the "lower basommatophorans." The 
second group includes the freshwater pul- 
monates, or "higher limnic basommatopho- 
rans." According to this view the Stylom- 
matophora are polyphyletic, although having 
all originated from the Archaeopulmonata. 
Harry (1964) slightly modified Burch's phyl- 
etic tree by adding a "pre-pulmonate" an- 
cestor to the Urbasommatophora [sic]. A 
similar framework of classification, also fol- 
lowed here, was adopted by Van Mol (1967), 
Hubendick (1978), Salvini-Plawén (1980), 
Boss (1982) and Tillier (1984), who restricted 
the term Basommatophora to Burch's 
"higher limnic basommatophorans." 

Quite a different view was proposed by 
Starobogatov (1976), mostly on the basis of 
the reproductive system. He reversed the di- 
rection of the evolutionary relationships 
within the pulmonates and considered the 
basommatophorans as derived from the sty- 
lommatophoran stock. Starobogatov did not 
consider the widespread fusion of the ganglia 
in the stylommatophorans, a condition that is 
considered derived. Reversal to a more dis- 
persed condition of the ganglia is very un- 
likely and has not been reported for other 
groups. 

Phylogenetic relationships within the Ello- 
biidae, although obscured by the presence in 
each subfamily of primitive and derived char- 
acters, can be elucidated by comparing the 
reproductive and nervous systems. Diauly, 
nonglandular condition of the palliai gono- 
ducts and ganglionic concentration on the 
nervous system are derived conditions (Gos- 
liner, 1981; Haszprunar, 1985, 1988; Salvini- 
Plawén & Haszprunar, 1987); I consider these 
features decisive in the interpretation of the 
degree of departure from the ancestral plan. 
A tentative phylogenetic tree elaborated on 
that basis is presented in Figure 401 and Ta- 
bles 5 and 6 (Appendix). 

Consistent patterns of organization al- 
lowed a clear delimitation of subfamilial 
boundaries. Five types of organization of the 
reproductive system were identified, corre- 
sponding to Morton's (1955c) subfamilial di- 
visions, for which they are named. First is the 
Pythiinian type, monaulic, with the anterior 
mucous gland and prostate gland running 
parallel to each other and covering the palliai 
gonoduct as far as the vaginal atrium. Sec- 
ond is the Ellobiinian type, diaulic, with the 
anterior mucous gland and prostate gland 
covering the palliai gonoducts for all their 
length. Third is the Carychiinian type, monau- 



312 



MARTINS 





Ringicula 



a 



Pythia 
Myosotella 
Ovate IIa 
Laemodonta 

Cassidula 



Carvchium 



Pedipes 
Creedonia 
Cremnobates? 
Micro trail a 

Pseudomelampus 
Marin и la 
LeuconoDsis 



Tralla 
Melampus 

Detracia 



Aurlculodes 
Elloblum 
Auricullnella 
Blauneria 



FIG. 401. 



WESTERN ATLANTIC ELLOBIIDAE 



313 



lie, with the palliai gonoduct glandular and 
the prostate gland concentrated distally in 
the gonoduct. Giusti (1975), in a sketchy rep- 
resentation of the reproductive system of 
Zospeum, left doubt whether the system is 
monaulic or diaulic, but the glandular appear- 
ance resembles the pythiinian or ellobiinian 
types; however, dissections of Carychium cf. 
thdentatum from the Azores using superficial 
staining with methylene blue (Martins, per- 
sonal observation) indicated an agglomera- 
tion of what appeared to be a prostate gland 
near the distal portion of the palliai gonoduct, 
thus substantiating Morton's (1955c) inter- 
pretation. Fourth is the Pedipedinian type, 
monaulic or incipient semidiaulic, with the 
anterior mucous gland and the prostate 
gland covering only the proximal half of the 
pallia! gonoduct. Fifth is the Melampinian 
type, advanced semidiaulic, with a very 
short, nonglandular spermoviduct and sepa- 
rated, nonglandular, long vagina and poste- 
rior vas deferens. 

Although not so discrete as in the repro- 
ductive system, patterns were found in the 
organization of the central nervous system, 
concerning the relative lengths of the various 
connectives. Three types were identified. The 
Pythiinian type has a wide visceral nerve ring 
and a long right parietovisceral connective. 
The Ellobiinian-Carychiinian type has a wide 
visceral nerve ring, sometimes with marked 
chiastoneury, and a very short right parie- 
tovisceral connective. The Pedipedinian- 
Melampinian type has a short visceral nerve 
ring; the connectives between the cerebral 
ganglia and the visceral nerve ring are longer 
and symmetrical in the Melampinae, whereas 
they are generally shorter in the Pedipedinae, 
with the right ones longer than the left ones. 

The phylogenetic relationships within the 
difterent subfamilies of halophilic Ellobiidae 
are better explained if one considers the 
Pythiinae as the representatives of the prim- 
itive core from which the Ellobiinae, the Cary- 
chiinae and the remaining taxa as a third 
group independently radiated. First, the 
Pythiinae have a monaulic, glandular palliai 
gonoduct and a wide visceral nerve ring. 
Pythia still has a very weak remnant of chia- 



stoneury and retains a functional open sper- 
matic duct. The presence of a palliai gland in 
species of Pythia, Cassidula, Ovatella and 
Laemodonta suggests a relationship of that 
group of the Pythiinae with the terrestrial 
Carychiinae. Secondly, the Ellobiinae must 
have separated from the primitive stock very 
early, for they retain the most primitive ner- 
vous system. The reproductive system is di- 
aulic; the palliai gonoducts, although glandu- 
lar in their entirety, separate immediately 
anterior to the seminal vesicle, eliminating the 
spermoviduct. Thirdly, the Pedipedinae and 
the Melampinae might have arisen from the 
same stock. In both subfamilies the visceral 
nerve ring is very short, concentrating the 
ganglia in the cephalopedal region. In the Pe- 
dipedinae there is some proximal concentra- 
tion of the antehor mucous gland and pros- 
tate gland, giving rise to a partly nonglandular 
palliai duct that is monaulic in most genera. In 
Leuconopsis and Pseudomelampus the vas 
deferens separates some distance before the 
female genital opening, giving rise to what is 
called here an incipient semidiaulic repro- 
ductive system [Visser's semidiaulic system], 
vaguely resembling a rudimentary step to- 
ward the condition in the Melampinae. In this 
subfamily the reproductive system is here 
called advanced semidiaulic. There is a very 
short spermoviduct, on which the inconspic- 
uous prostate gland is located, and the an- 
terior mucous gland has completely disap- 
peared. In Tralla the bursa duct inserts more 
distally in the vagina, a fact that suggests that 
there might have been a proximal migration 
of that structure and of the spermoviduct. 
The combination of ganglionic concentration 
and nonglandular, advanced semidiaulic pal- 
liai gonoduct indicates that the Melampinae 
are the least primitive ellobiids. 

The subfamilies, listed in order of increas- 
ingly derived characters, are Pythiinae, Ello- 
biinae, Pedipedinae and Melampinae. As 
stated above, however, primitive and derived 
characters occur in each subfamily. The 
Pythiinae, for example, live farther inland than 
any other halophilic ellobiid (Morton, 1955c); 
this habit is seen as a derived condition. 
Some Pedipedinae {Pedlpes, Creedonia) do 



FIG. 401 . Cladograms for Ellobiidae generated by PAUP from data in Tables 5, 6 (Appendix). A, Consensus 
of 703 trees, all characters included; B, Consensus of 1396 trees, excluding character G, status of sperm 
groove, a, Outgroup; b, Pythiinae; c, Carychiinae; d, Pedipedinae; e, Melampinae; f, Ellobiinae. O, Plesio- 
morphies (monauly, palliai ducts entirely glandular, wide visceral nerve ring); 1, Apomorphy diauly; 2, 
Apomorphy concentration of visceral nerve ring; 3, Apomorphy palliai ducts partly glandular; 4, Apomorphy 
incipient semidiauly; 5, Apomorphies advanced semidiauly and palliai ducts nonglandular. 



314 



MARTINS 



not resorb their inner whorls and are consid- 
ered primitive in this respect. The Melampi- 
nae retain a free-swimming veliger larva and, 
consequently, have a highly heterostrophic 
protoconch, which is a primitive feature. The 
occurrence of such a variety in the expres- 
sion of the different characters within the 
Ellobiidae obscures the tracing of a linear 
phylogenetic relationship for the family. I 
conclude with Morton (1955c) that the evolu- 
tion among the Ellobiidae is better under- 
stood as following a mosaic pattern, in which 
the organs and the mode of life evolve at dif- 
ferent rates in the various taxa. 

Zoogeography of the Ellobiidae 

The Recent Ellobiidae are a primarily trop- 
ical family, distributed in three centers. 

The first is the Indo-Pacific center, extend- 
ing from the East African coast to Polynesia. 
This center is characterized by large ellobi- 
ids, such as Ellobium, Cassidula and Pythia. 
Only four of the 21 genera of halophilic ello- 
biids are not represented in this center, the 
Mediterranean Ovatella and AuricuHnella, 
the Eastern Atlantic Pseudomelampus and 
the newly created West Indian Creedonia. 
Besides Ellobium s.s. and the other two gen- 
era that characterize this center, four others 
are endemic in the Indo-Pacific, Cylindrotis, 
known from the Philippines and Thailand 
(Brandt, 1974), Ophicardelus, from the Aus- 
tralian region, Allochroa, recorded from the 
Pacific Islands and from the Red Sea, and the 
widely distributed Auriculastra. 

The second is the West Indian center, 
which includes the Neartic and Neotropic 
regions and Ascension Island. The genus 
Melampus characterizes this center. Ten 
genera are present in the Western Atlantic, of 
which only the new genus Creedonia is en- 
demic. Of the 18 western Atlantic species 
seven belong to the genus Melampus. 

Wallace (1876) assigned with difficulty an- 
other mid-South Atlantic island, St. Helena, 
to his Ethiopian region, but he did not even 
mention Ascension Island. Rosewater (1975) 
noted that Ascension Island is very poor in 
endemic marine mollusks (only one subspe- 
cies and the new ellobiid species Leuconop- 
sis manningi) and that the malacofauna of the 
island contains even numbers of species 
from both sides of the Atlantic. The inclusion 
of Ascension Island in the West Indian center 
is justified by the presence of the Western 
Atlantic Pedipes mirabilis and of the new spe- 



cies Leuconopsis manningi. These are the 
only ellobiids reported from that South Atlan- 
tic island. 

The third is the Mediterranean center, 
which includes the Macaronesian Islands 
(Azores, Madeira, Canary Islands and Cape 
Verde Islands), is characterized by the en- 
demic Auriculinella and Ovatella, and also by 
the more widely distributed Pseudomelam- 
pus and Myosotella. Pseudomelampus is 
reported from South Africa [Melampus acino- 
ides (Morelet, 1889)] and Myosotella, repre- 
sented by the extremely variable and equally 
overnamed Myosotella myosotis, has be- 
come cosmopolitan. 

The tropical character of the ellobiids is 
well exemplified in their Western Atlantic dis- 
tribution. Of the 18 recorded species only 
three are reported from the American coast 
north of southern Florida, Melampus (M.) bi- 
dentatus, Melampus (D.) floridanus and the 
introduced European Myosotella myosotis. 

Bermuda was included by Wallace (1876) 
in his Alleghenian subregion of the Neartic, 
but it appears that the island should belong 
rather in the Antillean subregion of the Neo- 
tropical. Eight (67%) of the ellobiid species 
not represented on continental shores north 
of southern Florida were recorded from Ber- 
muda. 

Another interesting note is the record of 
Tralla (T.) ovula from the African coast. It ap- 
pears to be an isolated report, for the genus 
has not been reported from elsewhere in Af- 
rica; however, the 49 specimens collected by 
Dohrn in 1866 and deposited in the Museum 
of Comparative Zoology indicate that the 
species was not rare at llha do Principe, in 
the Gulf of Guinea. This West Indian species 
might have been transported to Africa in the 
ballast of ships, which I think was important 
in the dispersal of Myosotella myosotis as 
well. 

It is worth noting that both species of Pe- 
dipes, although broadly overlapping in the 
West Indies and Bermuda, overlap very little 
in Florida; I could not substantiate in any mu- 
seum collection or in my extensive collec- 
tions any record of Pedipes mirabilis from the 
Florida Keys. 

As noted in the remarks under the family, 
the fossil record of the Ellobiidae is relatively 
poor. It is interesting that the oldest known 
fossil ellobiids are the European Carychiopsis 
from the Paleozoic of France. This genus re- 
sembles the Recent terrestrial Carychium, 
which is known from the Jurassic of Asia, 



WESTERN ATLANTIC ELLOBIIDAE 



315 



Europe, America and West Indies (Zilch, 
1959). The Paleozoic of Europe contains fos- 
sils of the heavily dentate Traliopsis and the 
high-spired Stolidoma, which resemble some 
Recent examples of the Pedipedinae or the 
Pythiinae. They were most probably halo- 
philic, as were Rhytophorus and Melam- 
poides [Melampinaej from the Cretaceous of 
North America. It appears, then, that the el- 
lobiids had already invaded the terrestrial 
habitat through the Carychiinae during the 
Paleozoic, which implies that the group had 
separated very early from the prosobranch 
stem. 

Another interesting note on the paleogeog- 
raphy of the Ellobiidae is the presence of the 
Recent Indo-Pacific genera Ellobium and 
Cassidula in the Eocene of Europe, which 
suggests a Tethyan distribution. 

The Tertiary and Quaternary ellobiid gen- 
era of the West Indies are representatives of 
the Recent fauna both in their taxonomy and 
geographic boundaries. Marinula from the 
Pacific coast of Costa Rica (Dall, 1912), Pe- 
dipes from Venezuela (Gibson-Smith & Gib- 
son-Smith, 1979, 1985), Tralia from Venezu- 
ela (Gibson-Smith & Gibson-Smith, 1982) 
and Jamaica (Woodring, 1928), and Melam- 
pus (Detracia) from Virginia (Conrad, 1862) 
reflect the modern distribution of the respec- 
tive genera. 



ACKNOWLEDGMENTS 

I wish to express my gratitude to Dr. Rob- 
ert С Bullock, of the University of Rhode Is- 
land, for his patient advice and stimulating 
enthusiasm during the development of this 
work as a dissertation for the Ph.D and for 
allowing me to use material in his personal 
collection. I thank Dr. Ruth D. Turner and Dr. 
Kenneth J. Boss, Curators of the Department 
Mollusks of the Museum of Comparative 
Zoology, Harvard University, for their gener- 
ous help and their kindly allowing me to use 
the collection and library of that Department 
and never sparing their precious, expert ad- 
vice on the intricacies of the nomenclatorial 
problems. Also, I wish to thank the late Dr. 
Joseph Rosewater and the late Dr. Joseph 
Houbrick of the United States National Mu- 
seum in Washington, Dr. George M. Davis 
and Dr. Arthur Bogan of the Academy of Nat- 
ural Sciences of Philadelphia, Dr. William K. 
Emerson of the American Museum of Natural 
History in New York, Dr. John D. Taylor and 



Dr. Fred Naggs of the British Museum (Nat- 
ural History), Dr. Simon Tillier, Annie Tillier 
and Dr. J. -P. Hugot of the Muséum National 
d'Histoire Naturelle de Paris for kindly pro- 
viding access to their collections and for al- 
lowing me to use their computers for working 
with PAUP. I am indebted to Prof. Brian S. 
Morton of the University of Hong Kong and to 
Dr. A. Sasekumar of the University of Malay- 
sia, who provided me with preserved material 
of great importance for anatomical compari- 
sons, as well as to Dr. Claude Vaucher of the 
Muséum d'Histoire Naturelle de Genève for 
lending me Bourguignat's type material. The 
histological work was greatly simplified and 
enormously improved by the generosity and 
expertise of Dr. Paul Yevich and Mrs. Carolyn 
Barcsz Yevich of the E.P.A. Laboratory, Nar- 
ragansett Bay, Rhode Island, and by the con- 
tinuous assistance of Ms. Esther Peters; I am 
immensely grateful to them. I am most in- 
debted to the Rev. Joseph D. Creedon, Pas- 
tor of Christ the King Community, Kingston, 
Rhode Island, for his unreserved friendship, 
warm hospitality and exemplary patience in 
following and supporting the development of 
my research. I am also grateful to the Univer- 
sity of the Azores, to the Fundaçâo Calouste 
Gulbenkian and to the Instituto Nacional de 
Investigaçào Científica for their support in the 
various trips to the United States, England 
and France to prepare the revision of this 
work. Lastly, I wish to express my apprecia- 
tion for the loving support and continuous 
encouragement of my wife, Micéu. 



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