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THE0NAUTILUS

CONTENTS

Volume 124, Number 1

April 6, 2010

ISSN 0028-1344

Jason S. Higgs

Maren Watkins

Patrice Showers Corneli

Baldomero M. Olivera

Defining a clade by morphological, molecular, and toxinological criteria:

distinctive forms related to Conus praecellens A. Adams, 1854

(Gastropoda: Conidae) 1

Somsak Panha An anatomical note on Moellendorffia eastlakeuna (Mollendorff, 1882)

Chirasak Sutcharit a camaenid land snail from Vietnam (Gastropoda: Pulmonata:

Dang Ngoc Can Camaenidae) 20

Kristiina Ovaska Terrestrial gastropods from Haida Gwaii (Queen Charlotte Islands),

Lyle Chichester British Columbia, Canada, including description of a new northern

Lennart Sopuck endemic slug (Gastropoda: Stylommatophora: Arionidae) 25

Cleo Dihiei de Castro Oliveira How the number of hinge teeth may induce errors in the taxonomy of

Tatiana Huguenin Morales Nuculidae and Nuculanidae (Bivalvia) 34

Richard E. Petit A new species of Z eadmete (Gastropoda: Cancellariidae) from

Lyle D. Campbell South Carolina, a genus previously unknown in the Atlantic Ocean 41

Sarah C. Campbell

Monica A. Fernandez Current distribution of the exotic freshwater snail Helisoma dtiri/i

Silvana C. Thiengo (Gastropoda: Planorbidae) in Brazil 44

Fernando S. M. Bezerra

Lucia M. S. Alencar

Free Espinosa

Georgina A. Rivera-Ingraham

Jose C. Garcia-Gomez

Early stages of development in the endangered limpet Patella fermginea

Gmelin, 1791 (Gastropoda: Patellidae) 51

Notice

54

Sponsored in part by the State of Florida, Department

of State, Division of Cultural Affairs, the Florida Arts

Council and the National Endowment for the Arts.

NATIONAL

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FOR THE ARTS

TIIE NAUTILUS 124(1):1-19, 2010

Page 1

Defining a clade by morphological, molecular, and toxinological

criteria: distinctive forms related to Conus praecellens

A. Adams, 1854 (Gastropoda: Conidae)^

Jason S. Higgs*

University of Guam Marine Laboratory, UOG Station

Mangilao, GU 96923 USA

and

Department of Biology, University of Utah

Salt Lake City, UT 84112 USA

Maren Watkins*

Patrice Showers Corneli

Baldoinero M. Olivera1

Department of Biology, University of Utah

Salt Lake City, UT 84112 USA

ABSTRACT

We carried out a definition of the Conus praecellens A. Adams,

1854, species group using a combination of comparative

morphological data, molecular phylogeny based on standard

genetic markers, and toxinological markers. Prior to this work.

Conus praecellens was generally postulated to belong to a clade

of similarly high-spired, smaller species such as Conus pagoclus

Kiener, 1845, Conus memiae (Habe and Kosuge, 1970) and

Conus arcuatus Broderip and Sowerby, 1829. The molecular

phylogeny and toxinological data demonstrate that these earlier

hypotheses are incorrect, and that instead. Conus praecellens is

in a branch of Conus that includes Conus stupa (Kuroda,

1956), Conus stupella (Kuroda, 1956), Conus acutangulus

Lamarck, 1810, and surprisingly, some species that are mor-

phologically strikingly different. Conus mitratus Sowerby,

1870, and Conus cylindraceus Broderip and Sowerby, 1830.

A more careful analysis of the morphologically diverse forms

assigned to Conus praecellens suggests that from the Philippine

material alone, there are at least three additional species new to

science. Conus andremenezi. Conus miniexcelstis, and Conus

rizali. A reevaluation of protoconeh/early teleoconcii morphol-

ogy also strongly suggests that Conus excelsus Sowerby III,

1908, is related to these species. Together, the different data

suggest a clade including the 10 species above that we desig-

nate the Turriconus (Shikama and Habe, 1968) clade; there are

additional distinctive forms within the clade that may be sepa-

rable at the species level. The phylogenetic definition using the

multidisciplinary approach described herein provides a frame-

work for comprehensively investigating biodiverse lineages of

animals, such as the cone snails.

Additional keywords: Neogastropoda, Turriconus , 12SrRNA

sequences, phylogenetic analysis, exogenes

Support for this work was provided by grants from the

NII4GMS POl GM048677 (to BMO) and the NIHGMS Diver-

sity Supplement Fellowship 3 POl GM048677-13S1 (to JSB)

; To whom correspondence should be addressed: olivera@

biology, utah.edu

INTRODUCTION

The evolutionary histories of biodiverse Conus lineages

are a challenge to elucidate. In part this is because the

genus is so speciose (about 700 species) but also because

most prior data in the literature is morphological. The

usual approach is to characterize each species in the

lineage based on its shell morphology and to evaluate

phylogenetic relationships using additional anatomical

data, when available.

Prior attempts to divide Conus into subgeneric groups

have been based largely on shell morphology. In this

work, we focus on one particular branch of Conus that

includes the species known as Conus praecellens. Sev-

eral previous attempts to determine which species are

most closely related to Conus praecellens have grouped

C. praecellens with other high-spired forms (Figure 1)

that are collected in deep offshore locations. Some of the

specific prior hypotheses that have been proposed are

summarized in Table 1.

In the most comprehensive modem treatise on Indo-

Paeifie Conus species (Rockel et ah, 1995), Conus

praecellens is regarded as most closely related to Conus

acutangulus. In most of the schemes shown in Table 1

(Marsh and Rippingale, 1964; Okutani, 2000), Conus

praecellens is grouped together with Conus acutangulus

in the subgenus Conasprella Thiele, 1929. The designated

type of Conasprella is “C. cancellatus " ( = C. pagodus).

Another species generally thought to belong to this

subgenus is the Eastern Pacific Conus arcuatus. In one

of the proposals (da Motta, 1991), Conus praecellens and

Conus acutangulus are in two different subgeneric

groups: Conus praecellens in Conasprella and Conus

acutangulus in Kerniasprella Powell, 1958 (which this

author regards as a subgenus of the genus Profuncliconus

Kuroda, 1956). Among the species included with Conus

acutangulus in Kerniasprella are forms such as Conus

memiae and Conus nereis (Petuch, 1979), the latter

regarded by Rockel et ah, 1995 as a form of Conus

wakayamaensis (Kuroda, 1956). Thus, the high-spired

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THE NAUTILUS, Vol. 124, No. 1

Figure 1. High-spired Conus species previously postulated to be related to Conus praecellens-. Top from left: Conus acutangulus,

“typical form”; Conus acutangulus , “deep-water form”; Conus nereis. Middle from left: Conus praecellens, “Aliguay form”; Conus

praecellens, “sowerbii form”; Conus andremenezi new species (Holotype, MSI); Conus pagodus. Bottom from left: Conus

miniexcelsus, new species (Holotype, deposited at MSI); Conus rizali new species (Paratype 2, MSI); Conus arcuatus. All of the

specimens shown are from the Philippines, except lor Conus arcuatus. Measurements provided in Appendix 1.

J. S. Biggs et al., 2010

Page 3

Table 1. Previous taxonomic assignments of Conus praecel-

lens and Conus acutangulus.

Conus species including Conus praecellens were either

all grouped together in Conasprella, or were divided

into a praecellens/pagodus group (Conasprella) and an

acutangulus/memiae group (Kennasprella) .

These shell morphology-based suggestions can he

independently evaluated using molecular data. If only

morphological analyses are used, the resulting systemat-

ics may not reflect evolutionary trends as the traits may

be subject to selection forces that do not reflect common

descent. Distinguishing similarity by descent (reflecting

the phylogeny) from similarity directed by selection

(convergence or parallelism) is problematic without

independent data corroborating the morphological evi-

dence. Hence a widespread attempt to define biodiver-

sity using molecular markers, notably a segment of the

COI gene, has led to the “barcode initiative”. Although

this initiative has been widely implemented, workers who

need to identify field specimens require a more seamless

integration of the molecular with the morphological data.

Our first goal is to define a phylogenetic tree with

clades that reflect the branching pattern and in turn the

evolutionary history of the species. Molecular data pro-

vide independent evidence for such a phylogeny and a

useful organizational framework for in-depth studies of

species-rich groups. The morphological traits mapped

onto such a tree distinguish the respective roles of com-

mon descent and selection in the evolutionary process.

In this work, we focus on the definition of the putative

clade that includes Conus praecellens. Using 12SrRNA

sequences, we specifically evaluate which Conus species

are most closely related to Conus praecellens . In addition

to using a molecular phylogeny to assess morphology-based

taxonomy, we have gathered molecular data in the form of

the genes that encode toxins expressed in the venom ducts

of cone snails. As will be shown, these highly specialized

“exogenes” (Olivera, 2006) are useful in defining discrete

branches of a large biodiverse lineage such as the cone

snails. This three-pronged approach defines a more com-

plete picture of the evolutionary history of these biodiverse

cone snails with the result that previous morphologically

informed hypotheses may be more objectively assessed.

MATERIALS AND METHODS

Specimen Collection. Most forms in the Conus

praecellens complex are collected offshore from 30-250

meters in depth. The bulk of Philippine specimens

in collections assigned to this species were collected

(together with such species as Tibia fusus (Linnaeus,

1758) and Xenopliora Solaris (Kosuge and Nomoto, 1072)

around 1960, primarily from a few classical fish trawler

localities (Maqueda Bay in Samar Is, Tayabas Bay in

Luzon); at the time, these were mostly identified as Conus

sowerbii (see Reeve, 1849; Springsteen and Loebrera,

1986). Because other forms in the praecellens complex

are mostly from even deeper water, these were less well

represented in collections; most specimens available in

museums are poorly preserved and/or dead-collected.

However, the combination of gill net and hookah collec-

tions in the Cebu/Bohol area of the Central Philippines

and intensive small trawl collections around the Island

of Aliguay has increased accessibility to several forms in

the Conus praecellens complex. Some of these are smaller

specimens that were sparsely represented in earlier col-

lections. A range of live-collected specimens with pre-

served protoconchs has become available, which has

facilitated the reevaluation of the Conus praecellens spe-

cies complex.

Phylogenetic Analysis. We aligned sequences using

Clustal X (Larkin et ah, 2007) and refined by eye using

MaeClade (Maddison and Maddison, 2005). The tree

was inferred using MrBayes (Huelsenbeck et ah, 2001;

Ronquist and Huelsenbeck, 2003). The run comprised

1,000,000 generations with the first 25% of the sampled

generations discarded as burn-in trees. Two MCMCMC

runs (metropolis-coupled Monte-Carlo nrarkov-chain),

using four chains each, were used to thoroughly explore

tree space. Convergence of the likelihoods was deter-

mined by comparing the average standard error of the

difference (ASED) in split frequencies between the two

runs and by comparing plots of the log-likelihood after

the burnin to the end of the runs. Optimality was also

judged adequate when tire PSRL (Potential scale reduc-

tion factor) for the total tree length and for each model

parameter reached 1.00.

Identification and Sequencing of Genomic Clones

Encoding O-Superfamily Peptides. Genomic DNA

was prepared from 50 mg each of tissues of Conus acu-

tangulus, Conus mitratus, Conus pracellens, and Conus

stupa using the Centra PUREGENE DNA Isolation Kit

Kit (Gentra Systems, Minneapolis, MN) according to the

manufacturers standard protocol. These gendmie DNAs

were used as templates for polymerase chain reaction

(PCR) with oligonucleotides corresponding to conserved

5' intron and 3' UTR sequences of omega and delta

prepropeptides. The resulting PCR products were puri-

fied using the High Pure PCR Product Purification Kit

(Roche Diagnostics, Indianapolis, Indiana) following the

manufacturers suggested protocol.

Page 4

TIIE NAUTILUS, Vol. 124, No. 1

The eluted DNA fragments were annealed to

pNEB206A vector and the resulting products transformed

into competent DH5a cells, using the USER Friendly

Cloning Kit (New England BioLabs, Beverly, Massachu-

setts) following manufacturers suggested protocol. The

nucleic acid sequences of the resulting omega and delta

toxin-encoding clones were determined according to the

standard protocol for automated sequencing.

Morphometric Analysis. Using dial calipers, we mea-

sured maximum diameter (mm) and total length (mm;

including spire height) of species within the praecellens

complex. Relative diameter was calculated as the ratio of

maximum diameter to total length. All species were

represented by multiple samples. In view of the low

between-sample variation, we calculated a single mean

relative diameter for each species.

RESULTS

Systematic Descriptions of Three New Species

of Conus

by Baldomero M. Olivera and Jason Biggs

Superfamily Conoidea Fleming, 1822

Family Conidae Fleming, 1822

Subfamily Coninae Rafiuesque, 1815

Genus Conus Linnaeus, 1758

Conus anclremenezi Olivera and Biggs, new species.

(Figures 1, 2, 6)

Description: Biconical in shape, mature specimens from

25-53mm. Moderately solid, and with a relatively high

spire, and generally broader than most related forms

(D/L 0.47). Last whorl is broadly conical, with raised

spiral ribs that are not smooth but always undulating (and

in some specimens, the ribs seem to have arch-like pro-

tuberances, instead of a continuous smooth rib). Raised

ribs on the body whorl are well separated from each other,

with interstices that have axial scales between them.

The body whorl has an off-white ground color with

characteristic purplish-brown spots that occur in zones;

in the two darker zones, the spots generally cover more

spiral ribs and extend into the interspaces (although

there is considerable variation). The protoconch is decol-

lated in most specimens, but when preserved it is a

rounded conical shape, translucent, veiy light yellowish

brown or off-white; the protoconch is followed by two

white early teleoconch whorls that are lightly nodulose

and angled at the periphery. The spots begin to appear

on the periphery of the third or fourth teleoconch whorl,

and typically these are more closely spaced to each other

than are the larger spots in the later spire whorls.

Type Material: The Holotype is deposited in the

Marine Science Institute (MSI) at the University of the

Philippines; Paratypes are deposited at the Academy of

Natural Sciences ol Philadelphia, Philadelphia, Pennsyl-

vania (ANSP 421619); the Museum national d’Histoire

naturelle, Paris, France (MNHN 21131); the Field

Museum of Chicago, Chicago (FMHN 312461); the Har-

vard Museum of Comparative Zoology, Cambridge Mass

(MCZ 361611); Zoological Museum of Moscow State

University, Aloscow, Russia (Lc-37964) and The Bailey-

Matthews Museum, Sanibel, Florida (BMSM 38672)

(see Appendix or a complete listing ol paratypes).

Type Locality: The type locality for Conns anclremenezi

is Aliguay Island, Philippines, where most specimens

in the tvpe series have been collected by commercial fish-

ermen using small trawls at depths around 150 m. Another

established locality is off Panglao, Bohol, from Balicasag

Island to Momo Beach where the species has been col-

lected by tangle nets in deeper water (~200-300m).

Geographical Distribution: From the Central to

Northern Philippines, probably to Viet Nam and possibly

much further West (see discussion below). In the recent

book of Thaeh (2005), the specimen figured as Conus

praecellens (Plate 61, Fig. 34) is likely to be a specimen

of Conus anclremenezi.

Etymology: This species honors the memory of Andre

Menez, one of the giants of the field of toxinology.

Remarks: The sculpture on die spire whorls is diagnostic:

the spiral ribbons on the larger spire whorls are raised,

relatively narrow to very narrow, and always far apart. The

vide spacing on the spire whorls between narrow raised

spiral ribs is a diagnostic trait of this species; in most similar

forms, the spiral ribbons or ridges are much closer together

and are more like flattened ribbons, broad and shallow. The

broad shape, purplish-brown spots, undulating spiral ribs,

and widely spaced ribs on the spire are characteristic

features tiiat separate the species from similar forms.

When the protoconch is decollated, this species is

difficult to separate from some closely related forms that

are potentially variants of Conus praecellens. Most spec-

imens can generally be differentiated by the distinctive

purple-brown color, the broader shell, the widely spaced

spiral ribbons on the spire whorls, and when preserved,

the conical protoconch. Most specimens in the type

series come from Aliguay.

There is a group of Philippine specimens, not from the

type locality, which we tentatively assign to this species.

These were collected by the Musorstom expeditions

prmoted by the Museum national d’Histoire naturelle,

Paris, to Lubang Island/Mindoro. Several large mature

specimens ol Conus anclremenezi , all dead collected, were

examined. All of these were collected at depths between

160-198 meters; at more shallow collection stations, this

form was absent and a narrower Conus praecellens variety

was present. This provides a more accurate estimate of the

depth at which this species occurs.

Finally, there is a small specimen figured by Rockel

et al. (Plate 54, Fig. 14) that appears to be a juvenile of

Conus anclremenezi: if the identity of this specimen can

J. S. Biggs et al., 2010

Page 5

Figure 2. Two morphospecies with non-“praecellens-\i\ce" protoconchs from Aliguay. All ol the specimens shown are from Aliguay

Island, Philippines, except the lower left specimen which was collected from southern Japan. Top row: Conus andremenezi- Bottom

row: Conus miniexcelsus. For Conus andremenezi , the Holotype (left), Paratype 7 (second from right), and Paratype 11 (right) are

shown. For Conus miniexcelsus , the Holotype (second from right), Paratype 2 (third from right), and Paratype 18 (rightmost

specimen) are shown. All of the types figured are deposited at the Marine Science Institute (MSI), University of the Philippines.

Measurements provided in Appendix 1.

be verified, it extends the range of this species across the

entire Indian Ocean since the specimen is reported to be

from Somalia. Thus, although almost all of specimens

examined were from the Central Philippines, there is

strong evidence for the occurrence of the species in the

Northern Philippines, and the possibility that it may have

a geographic distribution that is much wider is raised by

the Somali specimen in the Raybaudi-Massila collection.

Conus miniexcelsus Olivera and Biggs, new species

(Figures 1, 2, 4, 6 and S)

Conus praecellens f. subaequalis. — Robin, 2008: 424,

fig. 14 (non Conus subaequalis , Sowerby III, 1870)

Description: A moderately small shell; adult size range,

25-37 mm. High-spired, with both spire and body whorl

Page 6

THE NAUTILUS, Vol. 124, No. 1

having a straight outline, making the shell narrowly

biconical. The larval shell has 3. 0-3.5 whorls, translucent

brownish or purplish. There are 9-11 teleoconch whorls,

the first three being ivory-white, without spots, providing

a notable contrast to the translucent-colored protoconch.

At around the fourth teleoconch whorl, broad brown-

ish spots appear, centered around the periphery. The

ground color is white, with chestnut-brown spots. On

the body whorl there are a series of flat spiral ribbons.

The shell pattern on the body whorl can be divided into

3-5 zones. The most posterior, next to the suture, are a

series of about 6 spiral ribbons with extremely fine chest-

nut brown spots. These are followed by a zone with 3

noticeably broader spiral ribbons that have deeper brown

and larger spots. In most specimens, this is followed by

three spiral ribbons that have a finer spotted pattern (but

not as fine as in the spiral ribbons in the first zone, closest

to the suture). The remainder of the shell towards the tip

is covered by spiral ribbons that are darker in color and

more heavily spotted; typically the first 3 to 4 are darker

than those towards the anterior end of the shell, although

there is considerable variation in this regard. In some

specimens, the light zone continues to the anterior of

the shell.

Type Material: The Holotype is deposited at the

Marine Science Institute at the University of the Philip-

pines, Paratypes are deposited at the Field Museum,

Chicago, Illinois (FMNII 312462); the Museum National

d’Histoire Naturelle, Paris, France (MNPIN 21132); the

Harvard Museum of Comparative Zoology, Cambridge,

Massachusetts (MCZ 361609); the Academy of Natural

Sciences of Philadelphia, Philadelphia Pennsylvania

(ANSP 421620); Zoological Museum of Moscow State

University, Moscow, Russia (Le-37965) and The Bailey-

Matthews Museum, Sanibel, Florida (BMSM 38673)

(see Appendix or a complete listing of paratypes).

Type Locality: Aliguay Island, Philippines. Most spec-

imens in the type series were collected by the commer-

cial small-trawl operations off Aliguay Island, at depths

of 30- 150m.

Geographical Distribution: Presently known from the

Central Philippines to Wakayama, Japan (Paratype #23).

Etymology: The specific epithet emphasizes some strik-

ing and unexpected similarities to Conus excelsus despite

the considerable disparity in size.

Remarks: A distinguishing characteristic of this species

are the spots on the whorls closest to the suture, which

are generally extremely line in pattern and greater in

number than for any other similar species, followed

by the thicker, darker brown spiral ribbons at the

center of the body whorl. These features are clearly

illustrated in the specimens shown in Figure 3. Conus

miniexcelsus is a distinct species, most easily confused

with Conus praecellens. However, as discussed above

and shown in Figure 3, the differences in protoconch

and early teleoconch morphology between the two spe-

cies are consistent distinguishing characters. This feature

puts Conus miniexcelsus in the same group as Conus

acutangulus, Conus andremenezi, and Conus excelsus

(except that the spire of Conus acutangulus has strong

tubercules at the sutures). Conus andremenezi is gener-

ally larger, with coarse spots that are purplish brown in

color instead of chestnut. Conus miniexcelsus is probably

most similar to Conus excelsus, although there is a strik-

ing difference in size at maturity. The two Japanese spec-

imens examined are more solid and chunky than the

Aliguay material. Figure 8 shows the different shape and

color of the protoconehs and the characteristic switch in

Conus miniexcelsus from a conical translucent purplish

brown protoconch, to the ivory white first teleoconch

whorls, and finally to the normal spotted pattern.

Conus rizali Olivera and Biggs, new species.

(Figures 1, 3, 6)

Description: The species is medium-sized; specimens

examined are 26-39 mm in length. The shell is biconic,

with an unusually tall, straight, and sharply pointed spire

and a straight-sided body whorl, sharply angled at the

shoulder. Outline narrow (D/L = 0.397 ± 0.011); The

larval shell has two whorls, and is praecellens- like but

somewhat proportionally broader than for most specimens

of Conus praecellens; this is followed by two teleoconch

whorls that have a characteristic white-matte surface,

somewhat crinkly; starting with the fourth teleoconch

whorl, there are 8-9 spotted spire whorls.

The body whorl is characterized by shallow spiral

ribbons with only a narrow interstitial space between

them; these are broadly spotted in light yellow-brown.

Characteristically, immediately below the periphery, the

first spiral ribbon lacks spots, leaving a white zone. Al-

though there is some variation, the spots are much ligh-

ter in color than in related forms (Paratype 2 almost

completely lacks spots in the body whorl).

Type Material: The Holotype is deposited at the

Marine Science Institute at the University of the Philip-

pines; Paratypes are deposited at the Academy of Natu-

ral Sciences of Philadelphia, Philadelphia, Pennsylvania

(ANSP 421621); the Harvard Museum of Comparative

Zoology, Cambridge, Massachusetts (MCZ 361610) and

in the Museum National d’Histoire Naturelle, Paris

France (MNIIN 21133) (see Appendix for a complete

listing of paratypes).

Type Locality: All type specimens were obtained from

commercial dealers in the Philippines, and the exact

collection locality of the types could not be verified.

Springsteen and Leobrara show a figure of Conus rizali

(labeled Conus subaequalis) indicating Punta Lugano,

Cebu, suggesting that these were probably collected by

fishermen using tangle nets at depths of 100-200m.

Geographical Distribution: Philippines.

J. S. Biggs et al., 2010

Page 7

Figure 3. Three distinctive forms with “praecellens- like” protoconchs. Top row is a series of Conus praecellens, "sowerbii form .

Bottom row is Conus praecellens, “Aliguay form”. In the middle row are two specimens of Conus rizali new species, the Holotype

(left) and Paratype 2 (right), both MSI. Measurements provided in Appendix 1.

Etymology: This species is named in honor of |ose

Rizal, the National Hero of the Philippines. Dr. Rizal,

who was executed by the Spanish Colonial Administra-

tion in 1898, collected shells as a hobby.

Discussion: Of all of the similar forms. Conus rizali has

the most narrow outline (D/L = 0.397 ± 0.011); spec-

imens of Conus praecellens from Aliguay, which

are generally narrower than the “Sowerbii form” have a

D/L = 0.44, and for Conus miniexcelsus ; (D/L = 0.416)

these are both narrower than Conus andremenezi.

Although Roekel et ah, put this species in synonymy

with Conus praecellens , we believe that it is a distinctive

form that can readily be separated from specimens

assigned to Conus praecellens. The narrower outline,

the shallow ribbons on the body whorl, and differences

in protoconch/early teleoconch moiphology separate

Conus rizali from other related forms. Conus rizali was

previously figured as Conus suhaequalis Sowerby III,

1870, by authors. This name was used by Springsteen

and Leobrera, and by Lim and Wee (1992); however,

the specimen recently figured by Robin (2008) as Conus

subaequalis is not Conus rizali but Conus minexcelsus.

A specimen was also figured by Roekel et al. (Plate 54,

Figure 6) but they refer this to Conus praecellens. Conus

rizali is sufficiently distinct so that it can immediately be

picked out from other related forms discussed elsewhere

in this article: the narrow outline of the shell sets it

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THE NAUTILUS, Vol. 124, No. 1

immediately apart, and in fact the form that is most

similar in outline is Conus gratacapi from Japan, which

is an unrelated species. This species has only been inter-

mittently collected over the last four decades, and never

in large numbers. As has been discussed in detail by

Rockel et al., and is shown in the original figure of

Sowerby (which Rockel et al., reproduced), the spec-

imens that we assign to Conus rizali are clearly not con-

specific with the figure of Conus subaequalis , which

likely refers to a different form in the Conus praecellens

complex.

Morphological Definition of Species in the Conus

PRAECELLENS COMPLEX: TWO “a/FVIEXCELSCS-LIKE” FORMS

In this section, we describe and define two distinc-

tive forms in the Conus praecellens complex from the

Philippines. As wall be defined in the Discussion, the

“ Conus praecellens complex” can be divided into two

broad groups on the basis of protoconch morphology,

the “ praecellens -like” forms and the “miniexcelsus- like”

forms.

The two miniexcelsus- like forms from Aliguay Island

(i.e., those with non-praecellens-like protoconchs), which

we proposed to designate as new species, are discussed

first. The Aliguay specimens of these two forms are

easily distinguishable from each other (see Figure 4).

Since both of these miniexcelsus -like forms were appar-

ently unnamed, these are formally described in the sec-

tion above. The appendix summarizes the individual type

specimens on which the new taxa are based.

Conus andremenezi Olivera and Biggs, new species

(Figure 2)

This form may be similar or identical to Conus bicolor

Sowerby I, 1833, which is a preoccupied name. Sowerby

then provided a new name in 1841, Conus sinensis.

Rockel et al., (1995) stated that “taxonomic status of

Conus bicolor/ Conus sinensis (Sowerby II, 1841)

remains disputable because the type specimen is lost

and the type figure (Plate 54, fig. 3) does not match C.

praecellens in a satisfying way: the pictured shell has a

comparatively low spire. . .is somewhat bulbous below

the shoulder and its color pattern consists of brown axial

flames. . .we favor synonomy with Conus praecellens.'

The figure shown by Rockel et al. (originally drawn from

“ Conus bicolor”) is similar to the species we describe

above as C. andremenezi ; we have not adopted the name

Conus sowerbii for this species because the syntype in

the British Museum does not appear to be nonspecific

with C. andremenezi.

We believe that Conus andremenezi is clearly dis-

tinguishable from typical Philippine specimens of

C. praecellens; first, the protoconch is not “praecellens-

like”; second, this form is generally broader and has a

characteristic purplish-brown coloration. Furthermore,

on the body whorl, there are raised but not flattened

spiral ridges that undulate, with a wade space between

ribbons with axial scales between the spiral ridges. More

consistently, the sculpture on the spiral whorls has nar-

row, raised ridges, widely spaced from each other. This

suite of characteristics consistently distinguishes this

species from C. praecellens of similar size (see Figure 1)

and from Conus miniexcelsus (see next species); Conus

rizali is even more distinctive from C. andremenezi.

There are a group of small Conus praecellens that are

most easily confused with Conus andremenezi; these are

discussed under Conus praecellens below.

Conus miniexcelsus Olivera and Biggs, new species

(Figure 2)

This very distinctive species is characterized by its rela-

tively narrow shell outline (D/L ~ 0.42 vs. 0.47 for C.

andremenezi), the multispiral protoconch of 2.5-3. 0

whorls, which is translucent and distinctly brownish or

purplish and contrasts in its color with the first 2. 0-2.5

teleoeoneh whorls that are ivory white. In most spec-

imens, these white whorls are smooth or have, at most,

nearly obsolete tubercles. This is followed by 6-10 spot-

ted teleoeoneh whorls that are grooved and have strong

axial structure so that the upper part of each spire

whorl has a distinctly tiled appearance. The body whorl

lias shallow spiral ribbons with regular, brown spots

that have a characteristic pattern described in the

Appendix in detail. The colored, translucent protoconch

contrasting in color with the first two shiny- white

teleoeoneh whorls, combined with the slender shape

and the very fine spotted pattern are diagnostic of this

distinctive species. There is considerable variation in

how dark the spots are; a range of variations is shown in

Figure 4. A full description of this new species was pro-

vided in the previous section; detailed measurements

of all the types are provided in the appendix. Almost all

specimens have been collected by small trawls in Aliguay

from 60-130 m, but occasional specimens have also

been collected using gill nets off Balicasag Island. One

specimen assigned to this species from southern Japan

is included in the type series (Figure 4). Figure 2

makes evident the generally finer pattern and narrower

shell shape of Conus miniexcelsus compared to Conus

andremenezi. In addition the spiral ribbons of the body

whorl of Conus miniexcelsus are smooth, but are dis-

tinctly crenulated in Conus andremenezi.

Overview and Description of the

“PRAECELLENS-LIKE FORMS”

Conus praecellens remains a confusing taxon, and the

scheme proposed below is not entirely satisfactory; mul-

tiple forms have been assigned to this species by various

workers. Even after the two “miniexcelsus- like forms”

are separated as new species, what remains still com-

prises a confusing set of specimens, most of which we

are provisionally retaining in C. praecellens. We believe

that the retention of diverse forms within C. praecellens

J. S. Biggs et al., 2010

Page 9

Figure 4. An illustration of the "miniexcelsus-hke complex”. Shown are five specimens (left five) and close-ups of their respective

protoconchs (right five). Left, top and bottom: Conus miniexcelsus (Paratypes 2 and 18, respectively), middle: Conus excelsus, and

right top and bottom: Conus acutangulus. Measurements provided in Appendix 1.

will prove to be only an interim solution, and new mor-

phologically similar species will be identified once a

more extensive molecular and morphological analysis

has been carried out over a wider suite of specimens

from a greater geographic range.

There is a widely illustrated specimen designated as

“a possible syntype” of Conus praecellens from the British

Museum. This is atypical ol specimens assigned to

C. praecellens from the Philippines. This possible syntype

from the China Sea is lighter in color and finer in sculp-

ture on the body whorl than either of the two major

Philippine varieties that we include in C. praecellens. The

first group, “the Aliguay form,” which is small and light

colored, has been extensively collected both by the small

dredge operations in Aliguay Island, and is the form illus-

trated in Figure 3. A second more variable group that we

refer to as the “sowerbii forms,” include larger specimens

that vary considerably in shell pattern, shape, and size.

These comprise most specimens collected by fish trawlers

in the period from 1955-1965, particularly from two local-

ities, Tayabas Bay and Maqueda Bay. A third group is that

referred to by previous authors as Conus subaequalis and

is described above as Conus subaequalis. The three forms

are shown in Figure 5.

Conus praecellens “Aliguay form”

(Figure 3)

The series of specimens that we assign to C. praecellens ,

“Aliguay form”, appears to be the closest to the type in

the BMNH in shell pattern; these have mostly been

collected in 30-80 fathoms off Aliguay Island, between

Mindanao and Bohol in the Philippines. The Philippine

specimens are smaller than the BMNH “syntype” (aver-

age size ~ 24mm); key features that distinguish this form

are a blunt, paucispiral protoconch of two whorls, the

relatively smaller size, and the chestnut color of the

spots. Details of the spire sculpture and body whorl that

are also diagnostic are delineated below.

The shells of this form (see Figure 5) typically have

2. 0-2. 5 protoconch whorls, the first being quite spherical

and inflated, and the second narrower and more elon-

gate. The first two teleoconeh whorls are typically

white and flattened compared to the protoconch whorls,

and they are knobbed on the periphery, while the two

Page 10

THE NAUTILUS, Vol. 124, No. 1

brunneus

eg,us Stephanoconus VZ

Dauciconus W

vittatus

IldVebCeilb

eticus .

— tenuistriatus

gr.?r)um g|ans Leporiconus W

Viitulinus W

acutangulus -< Turriconus W?

Rhizoconus W

■ partus

, - radiatus

■ laterculatus

■ obscui%s°grap us Gastridium F

jaspideus

Conasprella W

B.tippetti

Figure 5. Phylogenetic tree of some Conus species based on 12SrRNA sequences. Species shown in Figure 1 are indicated with

arrows. Branches are labeled with Bayesian confidence values (posterior probabilities expressed as percentages). These data clearly

separate Conus acutangulus and Conus praecellens from the Conasprella species with 100% confidence and join them with C. stupa

and C. mitratus with 97% confidence.

protoconch whorls are smooth. There are 8 to 9 whorls

spotted with a chestnut brown color, with the first one or

two spotted whorl(s) also knobbed. The early teleoconch

whorls are characterized by a deep spiral groove on the

upper section ol the whorl; these spiral grooves gradually

increase in number as the whorls get larger; these are

narrow furrows that can ire bisected by axial sculpture that

varies considerably in strength; in specimens where the

axial sculpture is strong, the area immediately adjacent to

the suture looks as il it were tiled, since the combination of

the spiral grooves and the axial sculpture divide the area

between grooves into square sections. The broader part of

the spiral whorl is smooth to the periphery; the lower

suture is below the sharply angled periphery.

Conus praecellens “sowerbii forms”

(Figure 3)

There are forms in the C. praecellens complex most com-

monly found in collections; most specimens were col-

lected by trawlers around I960 in great numbers in the

Maqueda and Carigara bays of Samar Island, and in

Tayabas Bay of Southwestern Luzon, from Jolo Island in

the Sulu Sea. The “sowerbii forms” are larger and more

densely spotted than the specimens of the “Aliguay form"

described above. There is considerable variation in shell

morphology: some specimens are slender and narrow with

line sculpture; others appear to be much broader at the

shoulders with an overall coarser sculpture. However,

when preserved, the protoconchs of all of these have

the typical highly inflated first whorl, with only two.

pearly white protoconch whorls. A range of specimens

collected from various Philippine localities, all with typical

“praecellens- like” protoconchs that are well preserved are

shown in Figure 5 (the contrast between these and the

“Aliguay form” is also illustrated in that figure).

Given the distinctive (and mutually similar)

protoconchs of both the Aliguay and the “sowerbii forms,”

we have provisionally assigned these in C. praecellens.

However, further characterization of both the radular and

gut morphology, as well as a molecular characterization,

may prove that these are distinct from each other, and that

there are additional separable species embedded in the

“sowerbii forms”, a possibility that clearly needs to be

further evaluated.

Conus praecellens , other distinctive varieties.

A smaller form of Contis praecellens was recently col-

lected by MNHN, off Aurora, Eastern Luzon, Philippines.

These specimens were notable because they were veiy

similar to Conus andremenezi, but much smaller. They

are easily separable from Conus andremenezi because

they have the typical “praecellens- type” protoconch.

These look veiy different from the two Conus praecellens

“forms” described above. We note that in general. Conus

andremenezi is a larger species; however, there have

been juvenile Conus andremenezi specimens collected

using lumum-lumum nets in the Camotes Sea, along

with specimens of the Conus praecellens , “Aliguay form,"

described above. It seems likely that only juvenile spec-

imens of Conus andremenezi are collected at this

J. S. Biggs et al., 2010

Page ] I

locality because lumun-lumiin nets were used, and it pre-

sumably takes longer than the three months lumun-lumun

nets are laid out for Conus andremenezi to reach full

maturity. These small specimens of Conus andremenezi

do have the characteristic protoconchs of that spe-

cies, though they are somewhat lighter in color than

the Alignay series. In contrast, the variety of Conus

praecellens collected off Aurora (trawled at 83 m depth)

have the praecellens -type protoconch. At the same site,

the MNHN expedition collected two dead, somewhat

eroded specimens, that were larger in size, in a trawl

189-307 meters in depth that are likely to lie true Conus

andremenezi.

In addition, a species was recently described as Conus

beatrix, Poppe and Tagaro, 2006. We have not had an

opportunity to examine the Holotype of this species; it

maybe that these represent a series of unusually pale spec-

imens, possibly continuous with the Conus praecellens

“Align ay form”, described above. If this were the case,

and further molecular evidence shows that these are sep-

arable from Conus praecellens , then these authors would

have provided a potentially valid species name for Conus

praecellens “Aliguay form.”

Conus rizali Olivera and Biggs, new species

(Figure 3)

This distinctive species was previously recognized by

Springsteen and Leobrera (1986) and by Lim and Wee

(1992) as morphologically separable from any of the

other forms assigned to C. praecellens or C. acutangulus.

In their treatment of this complex, Springsteen and

Leobrera (1986) provided a figure of this form, to

which the name Conus subaequalis Sowerby IIP 1870,

was assigned, with the locality Punta Engano, Cebu,

Philippines. This locality suggests that the specimens

they examined were collected by gill nets in deep water.

A similar specimen was illustrated by Rockel et al. (plate

54, figure 6) and labeled “ Conus praecellens" from

Davao, Philippines (likely collected by tangle nets off

Balut Island, Davao). In our description of Conus rizali

(see above), the name we propose for this form, we

discuss a number of distinguishing morphological char-

acteristics. The name assigned by both Springsteen and

Leobrera and Lim and Wee, Conus subaequalis does

not appear to refer to this form (Rockel et al. reproduce

the original figure of Sowerby which refers to a smaller

shell, broader in outline with seemingly more deeply

colored spots than Conus rizali.)

The slender, high-spired, and biconical shape of C.

rizali is similar to the Japanese Conus gratacapai , a poorly

understood, rare, deep-water species. Several museum

specimens of C. gratacapai were examined, including

some Paratypes of the latter. Several striking morphologi-

cal differences indicate that the two forms are not conspe-

cific. Most notably, C. gratacapai does not have the sutural

structure of C. rizali ; there is a smooth transition between

whorls in the former, but a peripheral overhang between

spire whorls in the latter. Anodrer obvious difference

are the light brown spots of C. rizali, which are absent in

C. gratacapai Pilsbry, 1904. The spire sculpture of the two

forms differs significantly as well.

Other “miniexcelsus -like” forms: Conus excelsus and

C. actangulus.

The presence of a translucent multispiral brownish

or purplish protoconch, followed by several ivory white

teleconch whorls is a striking morphological feature of

Conus minexcelsus. In this respect, two well-known spe-

cies are “miniexcelsus- like”: C. excelsus and C. acutan-

gulus. Both have the same characteristic translucent

protoeonch and ivory white early teleconch whorls (see

Figure 6). All of these forms have the body whorl cov-

ered by spiral ribbons. Tbe major difference is in the

highly nodulose whorls of C. acutangulus, versus the

smoother whorl of C. minexcelsus. Conus excelsus is some-

what intermediate in this respect. There are also the strik-

ing and obvious differences in size, C. excelsus being by

far the largest. Although the shells are different in pattern

and size at maturity in these three species (Figure 4), note

the similar purplish brown translucent protoconchs,

followed by the ivory white early teleoconch whorls before

the regular shell pattern is initiated. Typical Conus

acutangulus (Figure 4, top right) and the “deep-water

form” (Figure 4, bottom right) are both distinctly more

nodulose while there is a striking similarity between

Conus excelsus and Conus miniexcelsus in their proto-

conchs and early teleoconch whorls.

Conus excelsus Sowerby III. 1908

(Figure 4)

This is one of the largest species in the group (to over

100 mm). The protoconch consists of about 3.25 whorls,

with a maximum diameter of about 1 mm. The protoconch

whorls are grayish, and early teleoconch whorls are bright

white that then begin to have brown radial blotches of

varying size in the later whorls. Early teleoconch whorls

have one deep spiral groove, increasing to up to 4 spiral

grooves in the later whorls. Although body whorl can be

almost smooth, some specimens have variably spaced, axi-

ally striate spiral groups separated by granulose ribbons.

Most specimens in the Philippines are from Balut Island,

Davao, collected by gill nets at depths of approximately

100-150 fathoms. Although C. excelsus is strikingly differ-

ent in size, the body whorl sculpture, the protoconch and

early teleoconch whorls show such strong similarities to C.

miniexcelsus that a close genetic relationship between the

two species seems highly likely.

Conus acutangulus Lamarck, 1810

(Figure 4, 6)

Among Philippine specimens, there appear to be two

varieties of Conus acutangulus, the “typical form”

(Figure 4, top row, right), which conforms to the neotype

designated by Kohn (Kohn, 1981) and a variety that we

will refer to as the “deep-water form” (Figure 4, bottom

row, right). This is a well-known species, and the only

THE NAUTILUS, Vol. 124, No. 1

Page 12

O

Figure 6. Distinctive forms proposed to belong to the Turricomts elude. Top row (showing the shell and, in the inset above it, a

close-up of the corresponding protoconch), from left to right: Conus excelsus ; miniexcelsus (Holotype); acutangulus, “typical form”;

acutangulus, “deep-water form”; andremenezi (Holotype); praecellens , “sowerbii form”; rizali (Holotype); praecellens, “Aliguay

form”. Lower row, from left to right: Conus stupa- stupella ; mitratus ; cylindraceus. The protoconch of Conus stupa is not shown; it

is extremely eroded in the figured specimen. Measurements provided in Appendix 1.

issue is whether the two distinct forms described below

are conspecific or not

“Typical form” (description after Rockel et ah, 1995):

This is a small to medium sized shell; the larval shell is

multispiral with 3 to 4 whorls. The teleoconch whorls are

strongly tuberculate for at least the first eight post-nuclear

whorls, a distinctive characteristic. The body whorl has

strong spiral ribbons or ribs that are separated by grooves

with strong axial threads. The shell is largely brown,

except for small, scattered white blotches at the shoulder

and center. The aperture is white. This form is collected in

relatively shallow water, typically between 3-20 m. Divers

in Batangas Bay, Luzon, collected most Philippine spec-

imens; more recently divers in Nucnucan, Bohol, have

collected the typical form. Lully mature specimens are

2.5-38 mm in length, D/L ~ 0.50-0.53. Typical fully

mature non- Philippine specimens are also illustrated by

Rockel et al. 1995 (plate 54, figs. 19 and 21).

“Deep-water forms:” The deep-water varieties typi-

cally occur between 30 to 150 meters, and are collected

either by dredging or gill nets. These forms do not have

the brown to dark brown color of the typical variety, but

are mostly white with sparse light orange-brown or gray-

ish flecks. Generally smaller than the typical form, most

specimens are 16-22 mm in length. This form has been

collected in Aliguay and Pamilacan Islands. A compari-

son of available deeper- water specimens assigned to

C. acutangulus reveals considerable variation that needs

to be more carefully investigated and defined. These

forms clearly occur outside the Philippines; Rockel

et ah, illustrate a specimen from the Solomon Islands

(plate 54, fig. 17).

Molecular Phylogeny: Relationship of Conus

PRAECELLENS TO OTHER HlGH-SPIRED CONUS SPECIES

Most of the forms investigated in this article were

collected in the Central Philippines, primarily by gill

nets or trawlers offshore. A number of smaller Conus

species of similar shape, including several diverse forms

assigned to Conus praecellens , are collected in this way

(Ligure I ). As described above, in most taxonomic work,

Conus praecellens is either explicitly discussed or implic-

itly grouped with similarly shaped, high-spired, small,

J. S. Biggs et al., 2010

Page 13

deep-water Conus species even when authors do not

endorse a specific phylogenetic scheme (for example see

Robin, 2008; Rockel et ah, 1995; Walls, 1979).

Table I summarizes previously proposed taxonomy

based on shell morphology, which can be assessed using

molecular data. For comparison, a phylogenetic tree

based on 12S mitochondrial DNA includes Conus praece-

llens and C. acutangulus , along other vermivorous, mollu-

scivorous, and piscivorous Conus species (see Figure 5).

This molecular phylogeny assigns C. praecellens and

C. acutangulus to the same elade. The surprising, yet

clear-cut, result is that most other species proposed to

be included in Conasprella with C. praecellens by previ-

ous workers based on shell morphology actually cluster

in a branch extremely divergent from most Conus. The

type species of Conasprella , C. pagodus , is on this very

distant branch, which we refer to as the “ Conasprella

elade”. Additional molecular data support these findings

(Bandyopadhyay et ah, 2008). These data, discussed

below suggest that the degree of divergence makes it

untenable to keep these species (C. pagodus , etc.) within

the same genus as other Conus species.

Definition of a Clade Based on Morphological and

Molecular Data: The combination of the morphological

analysis of the various species and distinctive forms above

combined with the available molecular data (Figure 5)

provides a framework for defining the group of Conus

spp. most related to C. praecellens and C. acutangulus.

As discussed above, some of the superficially similar high

spired Conus species are not at all closely related based on

the molecular data. In the Philippines, there are ten spe-

cies and L2 distinctive forms which we assign to this group

that we designate the Turriconus clade (Conus excelsus =

Conus nakayasui , type species). A comprehensive taxo-

nomic revision of the genus Conus is currently being

carried out by A. Kohn; we suggest that Turriconus is a

distinct branch within the major group of species that

together, comprise the genus Conus.

The molecular work definitively excludes a number of

Conus spp. from Turriconus; clearly, species such as

Conus pagodus. Conus memiae, Conus nereis, and other

deep-water species with high spires such as Conus

boholensis (Petuch, 1979), Conus eugrammatus (Bartsch

and Rheder, 1943), as well as non-Philippine species such

as Conus jaspidcus (Gmelin, 1791) and Conus arcuatus,

though morphologically similar to C. praecellens, do not

belong in the Turriconus clade. The 10 species and 12

distinctive forms that comprise the Turriconus clade in

the Philippines are shown in Figure 6, and summarized

in Table 2; as outlined in the table, these fall into four

groups that will be discussed in turn.

The first group is the excelsus/ acutangulus group

(Group I), with four species and five distinctive forms.

This group includes the type of Turriconus, Conus

excelsus. The second is the praecellens group with two

species and three distinctive forms. The third is the

mitratus group of at least two species and fourth, the

stupa group.

Table 2. Morphologically distinctive “forms" in the Turrico-

nus clade ( Conus excelsus, type species).

Peptide toxins belonging to the O-superfamily have been

determined for these “forms."

The first group of species, the excelsus/acutangulus

group, is characterized by a generally conical protoconch,

without the spherical, inflated first protoconch whorl. The

protoconch is translucent, brownish purplish or light yel-

lowish in color; and followed by two or more, much whiter,

teleoconeh whorls. The four species in this group are

Conus excelsus. Conus miniexcelsus. Conus andrenienezi,

and the two forms of Conus acutangulus described above.

In the second group, the praecellens group (Group II),

the characteristic feature is a white protoconch of two

whorls, with the first protoconch whorl being inflated

and spherical (i.e., “praecellens- like”). The characteristic

shape of this protoconch is diagnostic of this group (as

shown in Figure 6); there may be more species than are

recognized here, since this is a rather variable assem-

blage of forms as is discussed above. C. praecellens and

C. rizali are the two species in this group, with at least

two distinctive forms assigned to C. praecellens .

The third group in Turriconus, based on molecular data

and expanded using morphological similarities, is the

Conus mitratus group (Group III). These species have

much more elongated body whorls than are found in the

two groups above. They seem to share the characteristic

white early teleoconeh whorls before the mature colora-

tion is expressed with the first group. On morphological

grounds alone, we assign two species to this group: Conus

mitratus and Conus cijlindraceus (Broderip and Sowerby,

1830). The molecular evidence in this paper is only pro-

vided for Conus mitratus; however, corroborative molecu-

lar evidence for Conus cijlindraceus has been obtained by

others (C. Meyers, personal communication).

The fourth group in the Turriconus clade is a subge-

nus ( Kurodaconus ) (Group IV) recognized as distinctive

by some workers; the molecular evidence suggests these

species should be included in Turriconus. There are two

species in this group, Conus stupa and Conus stupella; it

is the opinion of several workers on Conus that these

may not be separable species, since they always appear

to occur together. This suggestion needs to be further

evaluated. These forms differ from Groups I and II by

the smooth body whorl, while the species in these groups

have the spiral ribbons or ribs.

THE NAUTILUS, Vol. 124, No. 1

Page 14

The overall hypothesis, based on the combined molec-

ular and morphological data, is presented in Table 2. We

used this working hypothesis as a guide to analyze toxins

in the putative species of the Turriconus clade, from

which DNA samples were available (marked by asterisks

in Table 2).

Using Toxinological Markers to Evaluate the

Turriconus Clade: The hypothesis presented in Table 2

was experimentally tested using a toxinological analysis.

Since cone snails are venomous animals, they use toxins

in their venom to capture prey, defend against predators

and for competitive interactions. Since each species pre-

sumably has a different spectrum of prey, predators and

competitors, the genes encoding venom components are

“exogenes,” which diverge very rapidly as new species

evolve. The peptide toxins that are present in Conus

venoms are encoded by only a few gene superfamilies;

these are predicted to undergo accelerated evolution.

Conus peptide genes are examples of exogenes

( Olive ra, 2006); their gene products act exogenously,

targeting other animals (instead of acting endogenously

within the cone snail itself). A considerable amount of

prior work has demonstrated that each Conus species

has its own distinct complement of venom peptides, with

the same peptides not found in venoms of even closely

related species. What would be predicted when a group

of closely related species is analyzed is that the gene

products encoded by a particular conopeptide superfam-

ily will be highly related to each other, but not identical

in sequence. This toxinological prediction was used to

test if the species proposed to be in the Turriconus clade

do indeed have closely related (but not identical) toxins,

as would be expected for exogene products.

All species for which DNA was available were ana-

lyzed; since no complementary DNA (cDNA) samples

were available, the analysis had to be carried out on

genomic DNA. The gene superfamily used for the anal-

ysis was the O-superfamily; it is possible to determine

the sequence of the mature toxins because there is a

conserved intronic sequence that borders the mature

toxin region (see Materials and Methods) thus, PCR

primers can be used to determine peptide toxin se-

quences from each species. The O-superfamily has

diverged into two branches (Olivera et ah, 1999; Terlau

and Olivera, 2004) one hydrophilic, which includes the

to- and K-conotoxins from fish hunting cone snail venoms

(the “co-branch”) and the second highly hydrophobic;

in fish hunting cone snails this includes the 5 and

pO-conotoxins (the “8-branch”). PCR primers used to

amplify genes in each branch are different and therefore

toxin sequences can be separately obtained. This analysis

was carried out and the results are shown in Figure 7.

It is clear from the figure that representatives of all

four species groups, separated using our aforementioned

morphological/molecular phylogenetic analyses, yielded

homologous O-superfamily peptide sequences that fall

into both the to- and the 5-branches; all of which share a

high degree of sequence identity. Moreover, as predicted

Homologous Peptide Toxins from the O-superfamily

G> - screen

C. acutangulus At6.1

CGGRRAPCRQYIQCCSHSCNTFLGTCV*

C. praecellens Pr6.1

CG S PRARCRQY LQCC SRHC NKFLGMCV *

C. mitratus Mp6.1

CGGPQAPCRQY SQCCSRVCNKFFNKCR*

C. stupa Sa6.1

CG P PRARCRQY LQCC SRRC I KFLNMCM *

8 - screen

C. acutangulus At6.7

DSCLAGSEFCGFLKIGPPCCSGYCLFVCL*

C. mitratus Mp6.7

ECRANGATCGILKPGAKCCDGWCFFVCIG*

C. praecellens Ps6.7

RDD DCVAGGQG CGFPKI GGPCCSGKCFFVCT *

C. stupa Sa6.7

EC FPKDT FCGFPS SGAPCC SGWCFWCA *

Figure 7. Toxinological analysis. Predicted mature toxin

sequences from two distinct branches of the O-superfamily

of conopeptides for four members of Turriconus : Conus

acutangulus. Conus mitratus. Conus praecellens, and Conus

stupa. An independent comparison of the toxin sequences from

the two branches, the hydrophilic to and the hydrophobic 5,

each demonstrate the close relationship between the different

species of the Turriconus clade analyzed.

by the exogenomic hypothesis (Olivera, 2006), these

peptide sequences have diverged from each other.

Therefore, the postulated accelerated evolution of these

exogenes, which, in turn, is an indicator of species diver-

gence, is indeed observed.

DISCUSSION

This study has used three types of data: comparative

morphology, molecular phylogeny based on standard

gene markers, and toxinological markers (i.e., peptide

toxin sequences). This tlnee-pronged effort was aimed

at branch definition leading to a specific phylogenetic

hypothesis. As is typical, none of the individual data sets

were as comprehensive or complete as might be desired;

nevertheless, the combination made the phylogenetic

framework proposed a compelling one.

Morphological Evidence: Importance of the

Protoconch/Early Teleoconch. Springsteen and

Leobrera (1986), separated two forms in the C. pra-

ecellens complex from the Philippines, the commonly

trawled form (designated Conus sowerbii), and a sec-

ond, much more slender form, with lighter yellowish

brown spots, assigned to Conus subaequalis (op. cit,

pi. 71, figs. I, 2). This treatment wtis subsequently

adopted by Lim and Wee (1992). Thus, while Walls

(1979) and Roekel et ah, only recognized C. praecellens

and C. acutangulus, these workers recognized three

distinctive forms from the Philippines/Southeast Asia

J. S. Biggs et al., 2010

Page 15

(“C. sowerbii” (= C. praecellens), “ C.subaequalis and

C. acutangulus) .

One reason why the definition of forms has been chal-

lenging is because most available specimens did not have

good protoconch (or early teleoconch) whorl preserva-

tion. Philippine specimens in this group from many local-

ities have a dark periostracum layer covering the spire of

the shell, which is routinely removed by commercial shell

dealers using acid, a treatment that destroys key features

critical for morphological differentiation. In the analysis

below, we used these “compromised” specimens in our

morphometric analyses but focused primarily on the few

specimens with well-preserved protoconch and early

teleoconch whorls for discriminating between forms.

Once consistent differences in protoconch and early

teleoconch morphologies were established, additional

morphological characters were used to help separate dis-

tinctive forms. This general approach was used for the

morphological definition of forms described above.

The basic approach is illustrated in Figure 8, which

show two forms collected off Aliguay Island; these

have proven to be particularly illuminating. Both would

have been assigned by Roekel et al. (1995) to Conus

praecellens. In Figure 8, the specimen on the right is a

specimen of what we refer to as the “Aliguay form” of

C. praecellens ; the other specimen (on the left) is Conus

miniexcelsus new species. The top section ol Figure 8

shows the shells of the two specimens of approximately

same size. Although their shell patterns differ, the consid-

erable variation observed in this complex led to a rather

confused situation in the past. The major morphological

observation that changed this situation is illustrated in the

lower section of Figure 8, which shows a magnified view

of the well-preserved protoconch and early teleoconch

whorls of the two specimens; we believe that the differ-

ences depicted are sufficiently diagnostic to definitively

assign the specimens illustrated into two distinct groups

(i.e., Conus praecellens and Conus miniexcelsus). The

multispiral brownish protoconch of C. miniexcelsus con-

trasts with the protoconch of the specimen assigned to

C. praecellens; the early teleoconch whorls are also dis-

tinctively different. Using these as the major criteria for

separating forms makes it simpler to identify other shell

morphological characteristics that consistently differ, even

though each individual character might have a consider-

able range of variation. This approach has provided a

much more consistent suite of characters to allow a defi-

nition of different morphospecies.

Using these criteria, the Philippine forms previously

assigned to C. praecellens fall into two separable groups:

a group that has a characteristic protoconch of 2.0-2. 5

whorls, with a rounded and somewhat inflated first

whorl; the protoconchs of these forms are pearly-white;

we have referred to these as the “praecellens -like forms."

The specimens that do not have this very characteristic

type of protoconch, herein collectively referred to as the

“miniexcelsus- like forms”, have the first protoconch

whorl not rounded, nor inflated. The entire protoconch

of the latter generally has a more triangular (conical)

Figure 8. Comparison of two morphospecies collected in

Aliguay Island, Philippines. The specimen at the left is Conus

miniexcelsus (Holotype), and on the right is Conus praecellens ,

“Aliguay form”. Top: The whole shell. Bottom: Close-up of the

protoconch and first few teleoconch whorls.

outline when compared to the “praecellens -like forms;"

these protoconchs are typically translucent-brown, trans-

lucent-yellowish or off-white. Although this color can be

subtle, the contrast to the pure-white early teleoconch

whorls is usually diagnostic.

THE MOLECULAR EVIDENCE

A major conclusion from the molecular analysis is that

C. praecellens and C. acutangulus do not belong in the

Conasprella clade. Instead, they form a distinct branch

among the major group of species in Conus. Another

unexpected result from the molecular phylogenetic anal-

ysis is the other species. Conus stupa and Conus

mitratus, branch within the same well-supported clade

as C. acutangulus and C. praecellens. In particular.

Conus mitratus has strikingly different shell morphology

from C. praecellens and C. acutangulus. In all previous

taxonomic work. Conus mitratus and Conus stupa have

Page 16

THE NAUTILUS, Vol. 124, No. 1

been assigned to different subgenera from Conus

praecellens and Conus acutangulus .

The Contribution of Toxinological Markers. Our

starting point for defining the elade of cone snails that

includes Conus praecellens were the previous proposals

in the literature for subgenera (or genera, when Conus

was split into multiple genera) that included Conus

praecellens. In most proposals, Conus praecellens was, in

effect, proposed to be related to other high-spired, deep-

water species such as Conus pagodus, Conus memiae,

and Conus arcuatus , which are usually assigned to

Conasprella. In some of the prior hypotheses, this

group of species was split in two; e.g., Conasprella and

Kennasprella (da Motta, 1991), or Conasprella and

Endemnoconus (Okutani, 2000). Although these various

proposals differ in detail, they all group C. paraecellens

and C. acutangulus with species such C. pagodus,

C. memiae and C. arcuatus. However, both the molecular

phylogenetic results using standard molecular markers

and the exogenomic data using toxinological markers are

inconsistent with all of these hypotheses; only Conus

praecellens and Conus acutangulus appear to be closely

related to each other by the latter two criteria. All of the

other species previously grouped with Conus praecellens

in prior phylogenetic proposals based on shell morphology

are now assigned to a distant and different branch of

cone snails from Conus praecellens/Conus acutangulus

(see phylogenetic tree in Figure 2).

Instead, the combined data led to a new and strikingly

different phylogenetic framework for the Conus species

comprising the branch that includes Conus praecellens ;

this proposal is summarized in Figure 7 and Table 2. An

entirely unexpected set of species appears to be more

closely related to Conus praecellens (in Groups 3 and 4

in Table 2). These Conus species (C. stupa, C. stupella,

C. mitratus, and C. cylindraceus ) were never previ-

ously proposed to be in the same clade/subgenus as

C. praecellens and C. acutangulus.

The use of toxinological markers has buttressed the

molecular phylogenetic analysis. The presence of highly

similar peptide toxins that belong to the O-superfamily

of conopeptides indicates that the various groups that

branch together with Conus praecellens are indeed

related, using an independent toxinological data set.

THE TURR1CONUS CLADE: OVERVIEW

A more comprehensive morphological analysis reveals

that various distinctive forms previously assigned to

Conus praecellens are likely not conspecific; three new

species were described and additional distinct forms

defined. Thus, Conus praecellens and the newly described

species. Conus miniexcelsus. Conus rizali , and Conus

andremenezi are now proposed to be species in the same

clade.

Finally, the morphological analysis focused on the

importance of protoconch/early teleoconch whorl mor-

phology. These morphological characters strongly suggest

that Group I in Table 2 should include Conus excelsus

given its strikingly similar protoconch/early teleoconch

morphology to C. acutangulus and C. miniexcelsus.

Clearly, there is a difference in size: Conus excelsus is

much larger at maturity. We would predict that the

molecular phylogeny and toxinology of C. excelsus wall

reveal a particularly close affinity to Conus miniexcelsus

(which is, in part, the basis for the proposed name of the

latter). Unfortunately, Conus excelsus is rare and we

have been unable to obtain a live specimen to date.

However, we propose to call the entire group the

Turriconus clade, with C. excelsus as the type species.

In terms of species diversity, it would appear that

Groups 1 and 2 in Table 2 are the dominant species

groups of this clade — except for the differences in

protoconch morphology detailed above, they are all

high-spired species with the body whorls characterized

by spiral ribs or ribbons. Conus excelsus is the type

species of the subgenus Turriconus.

All three types of data used for this investigation need

to be expanded. A more extensive molecular phylogeny

needs to be carried out on all of the forms indicated in

Table 2, including, in particular, the designated “distinc-

tive forms” so that an evaluation of whether these are

separable species can be carried out. The new species

we have proposed need to be rigorously evaluated both

by the standard molecular markers as well as by their

toxin genes. More refined molecular phylogeny should

also allow a better resolution of how the various forms

in the proposed Turriconus clade are related to each

other and to other species of Conus. In addition, the

exogenomic analysis, while in agreement with the molec-

ular phylogeny, also needs to be extended to all of the

species in the Turriconus clade, as well as to other gene

superfamilies expressed in venom ducts (in addition to

the O-gene superfamily that was shown in Figure 8). The

determination of venom peptide sequences by this type

of analysis is, in itself, of considerable intrinsic value,

since it would allow the predicted gene products from

each species to be chemically synthesized and directly

tested for functional activity. Finally, the morphological

analyses to date are based only on shell morphology.

Clearly, other morphological features, particularly the

internal anatomy, need to be evaluated; these will serve

as an independent test of the phylogenetic hypothesis

presented. Potentially, mutually shared and distinctive

morphological features of species in this clade of Conus

may be discovered.

The interaction between the three prongs that are the

basis of the approach used in this manuscript has a

potential synergy that goes beyond clade definition. The

morphological analysis of distinctive forms within the

Conus praecellens complex identifies candidates that

may or may not be different species, separable from the

ones already recognized. Using standard molecular phy-

logeny will help to define this; however, using exogene

analysis should be even more definitive: if these were

indeed separable species, then none ol the toxin gene

products should exactly overlap in their sequence,

J. S. Biggs et ah, 2010

Page 17

Because of the hypermutation in exogenes that accom-

panies speciation events.

If a distinctive form was truly a separable species,

different toxin sequences would be predicted — if it

were merely a variant ol the same species, then identity

in most venom peptide sequences should be found

(except for allelic differences). In some of the well-

known species (e.g., Conus textile , Linnaeus, 1758, and

Conus striatus Linnaeus, 1758) that are distributed all

over the Indo-Pacific, it has been shown that major

venom peptides have the same sequence, even from

variants whose shells may be distinguishable from each

other because of the long period it may have taken for a

species to spread across the entire Indo-Pacific, from the

Red Sea to Hawaii.

The inclusion of exogenes in the investigation of bio-

diversity has a significance that goes beyond differentiat-

ing between morphologically closely related species.

The divergence of exogenes from one species to the next

is indicative of different biolog)', shaped by different

selection pressures. This is essentially a molecular read-

out of the deeper biological/historical/ecological differ-

ences between species that might look morphologically

similar. Thus, the characterization of toxin genes in the

case of Conus not only serves as a tool for branch defini-

tion, but is a potentially important entiy point toward a

more profound understanding of the biological differ-

ences between species, a molecular readout that could

provide insights into the complex changes that accom-

pany the speciation events that give rise to a biodiverse

lineage of animals such as the cone snails.

ACKNOWLEDGMENTS

This work was supported by Program project grant

GM48677 from the National Institutes of General

Medical Sciences. We are grateful to Adam Baldinger

of the MCZ, Philippe Maestrati and Philippe Bouchet,

MNHN, Paris, and Paul Callomon and Gary Rosenberg,

ANSP, for the loan of specimens used in this study. We

are grateful to Chris Meyers for making his sequences

for C. cylindraceus available to us.

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da Motta, A. j. 1991. A systematic classification of the gastropod

family Conidae at the generic level. La Conchiglia, Rome,

48 pp.

Huelsenbeck, J.P, F. Ronquist, R. Nielsen, and J.P. Bollback.

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Larkin, M.A., G. Blaekshields, N.P Brown, R. Chenna,

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Lim, C.F., and V.T.H. Wee. 1992. Southeast Asian Conus, a sea-

shells book. Seaconus Private Limited, Singapore, 100 pp.

Maddison, D.R. and W. P. Maddison. 2005. MacClade 4.08.

Marsh, J.A. and O.IP Rippingale. 1964. Cone Shells ol the

World. 3rd Edition. Jacaranda Press, Melbourne, 186 pp.

Okutani, T. 2000. Marine Mollusks in Japan. Tokai University

Press, Tokyo, 1221 pp.

Olivera, B.M., 2006. Conus peptides: biodiversity-based dis-

covery' and exogenomics. Journal ol Biological Chemistry

281: 31173-31177.

Olivera, B.M., C. Walker, G.E. Cartier, D. Hooper, A.D. Santos,

R. Sehoenfeld, R. Shetty, M. Watkins, P. Bandyopadhyay,

D.R., and Hillyard. 1999. Speciation of cone snails and

interspecific hyperdivergence ol their venom peptides.

Potential evolutionary significance of introns. Annals of

New York Academy of Science 870: 223-237.

Reeve, L.A. 1849. Monograph of the genus Conus. I,. Reeve

and Co., London.

Robin, A. 2008. Encyclopedia ot Marine Gastropods.

XENOPHORA and ConchBooks, Hackenheim, 480 pp.,

461 pis.

Rockel, D.. W. Korn, and A. |. Kohn. 1995. Manual of the

Living Conidae (Vol. 1: Indo-Pacific Region) Verlag

Christa Hemmen, Wiesbaden, 517 pp.

Ronquist, F J.P. and Huelsenbeck. 2003. MrBayes 3: Bayesian

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Shikama, T. and T. Habe. 1968. A New Japanese Cone,

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Springsteen, F.J. and F. M. Loebrera. 1986. Shells of the Phil-

ippines. Carfel Seashell Museum, Manila, 377 pp., 100 pis.

Terlau, H. and B.M. Olivera. 2004. Conus venoms: a rich

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Page 18

THE NAUTILUS, Vol. 124, No. 1

APPENDIX

Baldomero M. Olivera and Jason S. Biggs

Conus andremenezi, summary of type specimens (Figures of types are cross-referenced)

J. S. Biggs et al., 2010

Page 19

APPENDIX

(Continued.)

Abbreviations: MSI, Marine Science Institute, University of the Philippines, Quezon City, Philippines, ANSP, Academy of Natural

Sciences, Philadelphia, PA, USA; MNHN, Museum national d’Histoire naturelle, Paris, France; MCZ, Museum of Comparative

Zoology, Harvard University, Cambridge, MA, USA; BMSM, The Bailey- Matthews Shell Museum, Sanibel FL, USA; FMHN, Field

Museum of Chicago, Chicago IL, USA; Lc, Zoological Museum of Moscow State University, Moscow, Russia; *, These specimens wall

be deposited in public museums, but have not yet been assigned.

THE NAUTILUS 124(l):20-24, 2010

Page 20

An anatomical note on Moellendorffia eastlakeana

(Mollendorff, 1882) a camaenid land snail from Vietnam

(Gastropoda: Pulmonata: Camaenidae)

Somsak Panha

Chirasak Sutcharit

Animal Systematic Research Unit

Department of Biology

Faculty of Science

Chulalongkorn University

Bangkok, 10330, THAILAN D

[email protected]

Dang Ngoe Can

Department of Zoology

Institute of Ecology and Biological Resources

18 Hoang Quoe Viet Road

Can Giay, Hanoi, VIETNAM

ABSTRACT

Newly collected specimens of Moellendorffia eastlakeana

(Mollendorff, 1882) expand the known range of this species into

Vietnam. Using these new Vietnamese and existing museum

samples we have re-described the species including new infor-

mation on radula and genital anatomy. Comparison with the

type material of M. callitricha (Bavay and Dautzenberg, 1899)

from Vietnam suggested M. callitricha is a junior synonym of

M. eastlakeana.

Additional keywords: Gastropoda, pulmonate, Traumatophora,

Chloritis, T ri ch elix

INTRODUCTION

The land snail genus Moellendorffia Ancey, 1887, has a

wide distribution in southeastern China, Hong Kong and

Vietnam. The detached peristome, descending aperture

with denticles, and hirsute shell with external furrows,

confer a very distinctive morphology on the shells

(Pilsbry, 1890, 1895, 1902, 1905; Yen, 1939; Azuma,

1982).

Currently, seven species are recognized within this

genus, namely: M. trisinuata (von Martens, 1867),

M. eastlakeana (Mollendorff, 1882), M. hensaniensis

(Gredler, 1885), M. loxotata (Mabille, 1887), M. messageri

(Bavay and Dautzenberg, 1899), M. spurca (Bavay and

Dautzenberg, 1899), and M. depressispira (Bavay and

Dautzenberg, 1908) (Pilsbry, 1905; Zilch, 1966; Richard-

son, 1985).

Originally, Moellendorffia was placed by Pilsbry (1890)

in a section of Helix (Stegodera) Martens, 1876, then

reclassified by Pilsbry (1894) as a subgenus ol Heli-

codonta Ferussac, 1819, and finally (Pilsbry, 1905) as a

distinct southeastern Chinese and Indo-Chinese genus

related to Stegodera and allied to Chloritis Beck,

1837. Likewise, Trichelix Ancey, 1887, was originally

placed by Pilsbry (1905) along with Moellendorffiella

Pilsbry, 1905, as subgenera within Moellendorffia , and

Traumatophora Ancey, 1887, as a subgenus of Stegodera.

Subsequently, Schileyko (2003) recognized Trichelix

as a genus distinct from Moellendoiffia and Zilch (1959)

separated Traumatophora as a genus distinct from Stego-

dera on the basis of the possession of a dextral shell with

apertural teeth.

The early descriptive work on Mollendorffia was

restricted to shell i Morphology (e.g., Pfeiffer, 1862;

Mabille, 1887; Bavay and Dautzenberg, 1899; 1908,

Pilsbry, 1902; 1905). Subsequently, Habe (1957), Azuma

(1982), and Schileyko (2003) provided some additional

anatomical information for M. trisinuata and Trichelix

eucharista (Pilsbry, 1902) (= M. (Trichelix) eucharista ).

In this article, we examine specimens of M. eastlakeana

collected from a forest reserve in northern Vietnam and

compare them to museum material originally collected

from other locations.

MATERIALS AND METHODS

We examined three specimens of M. eastlakeana collected

in May 1999 from the Huu Lien Nature Reserve, Lang

Son Province, northeastern border of Vietnam, which are

now deposited in the Chulalongkorn University, Museum

of Zoology (CUMZ). Type and other materials were criti-

cally examined in the Senckenberg Museum, Frankfurt

(SMF) and Museum National d’Histoire Naturelle, Paris

(MNHN). Terminology for soft anatomy follows that of

Habe (1957) and Schileyko (2003). The terms “proximal”

and “distal” refer to a position relative to the genital ori-

fice. Methodology for whorl counts and shell measure-

ments follow Kerney and Cameron (1979).

Abbreviations: at, atrium; e, epiphallus; fl, flagellum;

fo, free oviduct; gd, gametolytic duct; gs, gametolytic

S. Panha et al., 2010

Page 21

sac; hw, head wart; ov, oviduct; p, penis; pp, penial

pilaster; pr, penial retractor muscle; pv, penial verge;

v, vagina; vd, vas deferens; vp, vaginal pilaster.

SYSTEMATICS

Family Camaenidae

Genus Moellendorffia Ancey, 1887

Type species: Helix trisinuata von Martens, 1867,

Hong-Kong, China; by subsequent designation ol Pilsbry

(1905: 64).

Diagnosis: Shell medium size (11.5x19.5 mm), de-

pressed, rather thin, umbilicate and corneous to brown-

ish. Spire low to slightly convex; embryonic shell nearly

smooth; subsequent whorls granulated and with short to

long periostracal hairs. Last whorl rounded to shoulder

and suddenly descending anteriorly. Aperture trigonal

or squarish, entirely free from preceding whorl; usually

with barriers inside and externally marked with furrows.

Peristome expanded and continuous. Penis and epi-

phallus long, flagellum short and vagina long. Penial

wall with longitudinal pilasters. Radula with triangular-

shaped teeth.

Moellendorffia eastlakeana (Mollendorff, 1882)

Helix eastlakeana Mollendorff, 1882: 185 (Tai-mo-shan,

Kwangtung, China (= Hong Kong): Lectotype SMF 8328

by Yen, 1939); Mollendorff, 1885: 391, pi. 10, tig. 18.

Ancey, 1887: 64

Helix (Moellendorffia) eastlakeana. — Pilsbry, 1890: 12, 13, pi. 1,

figs 21, 22; Pilsbry, 1895: 290.

Stegodera eastlakeana. — Pilsbry, 1890: 310 (figure legend),

pi. 1, figs 21, 22.

Helix (Moellendorffia) callitricha Bavay and Dautzenberg,

1899: 35, pi. 1, figs 6, 6b (That-Khe near Lang Son,

Vietnam).

Moellendorffia eastlakeana . — Pilsbry, 1905: 65; Yen, 1939: 125,

228, pi. 13, fig. 3 (Lectotype SMF 8328); Richardson,

1985: 184.

Moellendorffia callitricha. — Pilsbry, 1905: 66; Richardson,

1985: 183.

1 mm 1 mm 5 mm

Figures 1-4. Shell characteristics of Moellendorffia eastlakeana , CUMZ 2547. 1. Shell morphology. 2. Shell surface structure and

showing the bristles on the periostracum. 3. Protoconch sculpture 4. Apertural lamellae.

THE NAUTILUS, Vol. 124, No. 1

Page 22

Moellendorffia (Moellendorjfia) eastlakeana. — Zilch, 1966: 210,

pi. 6, fig. 52 (Lectotype SMF 8328).

Material Examined: Tai-mo-shan, Hong Kong: Lee-

totype SMF 8328, Paralectotype SMF 8329 (2 shells);

Huu Lien Nature Reserve, Lang Son Province, Vietnam:

CUMZ 2547 ( I specimen), CUMZ 2549 (2 shells); That-

Khe, Tonkin, Vietnam (1 shell), MNHN Holotype of

“ callitricha ”; That-Khe, Tonkin, Vietnam (2 shells),

Denis collection (NMHN); That-Khe, Tonkin, Vietnam

(I shell), Staadt collection (NMHN); Tonkin, Vietnam

(1 shell), Messager collection (NMHN); Tonkin, Viet-

nam (2 shells), Messager collection (NMHN)

Measurements: From 10 specimens analyzed; shell

height ranged from 12.4 to 14.7 mm (mean 13.5±1.0

mm); shell width ranged from 20.8 to 23.9 mm (mean

22. 0±1. 2); and whorl count ranged from 6.0 to 6.1

whorls.

Shell: Shell (13.5 mm height, 22.0 mm width) slightly

thin, translucent, depressed globose and deeply umbili-

cate. Spire flat to convex. Shell brownish to light brown;

upper surface with long hairs (Figures I, 2); lower sur-

face with short hairs, few hairs around umbilicus. Shell

surface rough, rows of tubercles running obliquely anil

descending, relatively smooth around umbilicus. Embry-

onic shell large and with very fine growth lines (Figure 3).

Whorls 5-6, slightly convex and increasing regularly;

suture depressed. Last whorl rounded and little con-

vex below periphery. Aperture ear-shaped; lip margin

light brown and continuously expanded; externally with

furrows. Peristome free from preceding whorl and

abruptly descending. Aperture brownish inside with

well -developed, whitish, and semi-circular palatal and

basal lamellae located closed to apertural lip. Two exter-

nal furrows align with the internal apertural denticles.

Parietal callus thickened, elevated, emarginated and

obtusely projecting inward (Figure 4).

Genitalia: Atrium (at) short; penis (p) long; proxi-

n i ally with short penial verge and folded at penial verge

based; distally long and somewhat slender. Epiphallus

(e) shorter than penis. Flagellum (fl) short, small and

without appendix. From free oviduct, vas deferens (vd)

follows vagina and penis and connects distally on

epiphallus. Penial retractor muscle (pr) thin and veiy

long (Figure 5).

Internal wall of penis ribbed by series of swollen lon-

gitudinal pilasters (pp) (Figure 6). Smooth pilasters line

introverted penial chamber and encircle penial verge tip.

Penial verge (pv) short, conic and smooth (Figure 6).

Vagina (v) of similar length to penis, cylindrical and

held in position by connective tissue attached to foot

floor. Slightly swollen proximally; more slender distally.

Gametolytic duct (gd) as wide as gametolytic sac (gs) for

most of its length but narrows before gemetolytic sac.

Free oviduct (fo) short; oviduct (ov) small (Figure 5).

Internal wall of vagina possess several longitudinal

vaginal pilasters (vp) with smooth pilaster surfaces

(Figure 6).

Animal: Live animal covered with blackish reticulated

skin and dorsally with whitish stripe in middle ol the

Figures 5-7. Reproductive system of Moellendorffia eastlakeana , CUMZ 2547. 5. General view ol the genital system. 6. Interior

structure of the atrium, penis and vaginal chamber. 7. Dorsal view showing head wart.

S. Panha et al., 2010

Page 23

body. A small curve-shaped head wart (hw) is located

between the posterior tentacles (Figure 7). Foot narrow

and long; mantle edge grayish; tentacles gray, and lower

tentacles paler. Mantle cavity with blackish pigmenta-

tion. Live snails possess short to long periostracal hairs,

which mostly break off after death.

Radula: Teedi arranged in anteriorly pointed V-shaped

rows, each row contains about 70 (34-(15-17)-l-( 15-17)-

35) teeth. Central toodr triangular with minute eetocones.

Teeth become taller laterally. Lateral teeth tricuspid;

endocones and eetocones small and located half way

along tooth length (Figure 8). From tooth 16 to 17 out-

ward lateral teeth, the marginal ectocone originates from

the tooth base (Figure 9). Marginal teeth rather small,

tricuspid and aligned obliquely; endocone becomes taller

than mesocone; ectocone located basally (Figure 10),

sometimes divided into two or three cusps in outermost

teeth.

Distribution: Moellendorffia eastlokeana was previ-

ously known only from the type locality: Tai-mo-shan,

Hong Kong (Mollendorff, 1882, 1885; Pilsbry, 1890;

Yen, 1939; Zilch, 1966). Our material was collected from

Huu Lien Nature Reserve, Lang Son Province, north-

eastern border of Vietnam.

Remarks: On examination of the holotype of M. calli-

tricha and other topotypic material identified as this

species, the only detectable difference was a slightly ele-

vated spire relative to that of the lectotype of M. cast-

lake ana and other material recognized as M. eastlokeana.

On this basis we consider M. callitricha to be a junior

synonym of M. eastlokeana.

The locality characteristic of our sampling is mon-

soonal karst landform with high humidity. The sn; xils

occurred among the tropical moist deciduous forest.

There was rain before the time of our visit in May, 1999.

The snails were active, crawling on moist rotten logs.

Moellendorffia (M.) eastlokeana is distinctly different

in shell morphology from M. (M.) messaged (Bavay and

Dautzenberg, 1899), which occurs in the same area. The

latter species has a much smaller shell (about 8 mm

height; 14 mm width), flattened spire and shouldered

last whorl .

DISCUSSION

The newly collected material from Vietnam presents

valuable additional information for the taxonomic revi-

sion of Moellendoijfia and it allies. The presence ol

shell apertural lamellae and shell external furrows appear

as common shell characters among Moellendoijfia ,

Trichelix, and Moellendorffiella.

In consideration to the generic relationship, the pres-

ence ol lamellae and external furrows could be com-

mon characters among Moellendorffia, Trichelix, and

Moellendorffiella. The long epiphallus, short flagellum,

and triangular shape of the radula central tooth in both

Figures 8-10. Scanning electron micrographs of Moell-

endorffia eastlokeana radula, CUMZ 2547. 8. Central teeth

with the first to the third lateral teeth (black arrows indicate

endocone and ectocone). 9. Lateral teeth with the tricuspid

marginal teeth transition. 10. Marginal teeth. Central tooth is

indicated by “C” and the other numbers indicate the order of

lateral and marginal teeth.

Page 24

THE NAUTILUS, Vol. 124, No. 1

Trichelix and Moellendorjfia (Habe, 1957; Schileyko,

2003) may support their having a close relationship.

The parietal callus free from a preceding whorl, with

aperture lamellae, ear shaped aperture, and long hairs

are possibly the distinctive characters of Moellendorffia

sensu stricto. The position of two furrows (upper and

lower periphery), parietal callus thickened at the edge,

and tuberculated penial wall are probably the unique

characteristics of Trichelix. Unfortunately, the anatomy

of species of Moellendorjfiella is still lacking for

comparison, but the differences lie tween shells of

Moellendorffiella and Moellendorffia are the shouldered

last whorl, flattened spire, parietal callus shortly

attached to penultimate whorl, and rounded aperture

(Pilsbry, 1890, 1905). These differences support the dis-

tinct generic position of Moellendorffia, Trichelix, and

Moellendorffiella as proposed by Schileyko (2003).

However, with so few samples and, especially, so few

different species and informative morphological charac-

ters, the exact phylogenetic relationships remain equiv-

ocal. To better resolve the exact phylogeny, we suggest

that the anatomical examination from more localities

within each species range and from different species

required is still insufficient, however a molecular based

phylogenic approach is required in conjunction with

morphology traits.

ACKNOWLEDGMENTS

We thank F. Naggs (NHM, London), R. Janssen (SMF,

Frankfurt), and P. Bouehet and V. Heros (MNHN, Paris)

for permitting S.P. and C.S. to investigate type materials,

and FN. for critical comments on the manuscript. We

are especially grateful to S. Natsupakpong, P. Tongkerd,

N. Pattaramanon, and S. Pholkoksung for providing

important literature and assistance in the field. This

project was funded by the Thailand Research Fund (TRF),

the Thai-French Project TRF-CNRS (BRT 245005), the

RES-A1B1-7, the SP2-TKK2555-PERFECTA, and the

Darwin Initiative Project (DEFRA).

LITERATURE CITED

Ancey, C.F. 1887. Description of new genera or subgenera of

Helieidae. The Conchologists Exchange 1: 64.

Azuma, M. 1982. Colored illustrations of the land snails of

Japan. Hoikusha, Japan, i-xvi, 1-343 pp, pis 1-63.

Bavay, A. and P. Dautzenberg. 1899. Descriptions d’espeees

nouvelles de l'lndo-Chine, II. Journal de Conchyliologie

47: 28-55, pis 1-3.

Bavay, A. and P. Dautzenberg. 1908. Molluseorum terrestrium

Tonkinorum diagnoses. Journal de Conchyliologie 56:

229-251.

Habe, T. 1957. Anatomy of Moellendoiffia (Trihelix) euch-

aristus (Pilsbry). The Nautilus 71: 8-9, pi. 1.

Kerney, M.P and R.A. D. Cameron. 1979. A field guide to the

land snails of Britain and north-west Europe. Collins,

London, 288 pp.

Mabille, M.J. 1887. Sur quelques mollusques du Tonkin. Bul-

letins de la Societe Malacologique de France 4: 80-164,

pis 1—4.

Mollendorff. O. von. 1882. Diagnoses specierum novarum

chinae meridionalis. Jahrbiieher der Deutsehen Malako-

zoologischen Gesellschaft 9: 179-188.

Mollendorff. O. von. 1885. Materialien zur fauna von China

(Die Auriculaceen, Naehtrage und Beriehtigungen).

Jahrbiieher der Deutsehen Vlalakozoologisehen Gesell-

schaft 12: 349-398, Tafel 9-11.

Pfeiffer, L. 1862. Descriptions of thirty six new land shells from

the collections of H. Cumming, Esq. Proceedings of the

Zoological Society of London 1862: 268-278, pi. 36.

Pilsbry, H.A. 1890-1891. Manual of Conchology, Series 2, Vol-

ume 6. The Academy of Natural Sciences of Philadelphia,

Philadelphia, 1-324,' pis 1-69.

Pilsbry, H.A. 1893-1895. Manual of Conchology, Series 2, Vol-

ume 9. The Academy of Natural Sciences of Philadelphia,

Philadelphia, iii-xlvii, 1-366, pis 1-71.

Pilsbry, II. A. 1902. New land Mollusca from Japan and the Loo

Choo islands. Proceeding of the Academy of Natural Sci-

ences of Philadelphia 53: 344-353.

Pilsbry, H.A. 1905. Notes on Moellendoiffia and Stegodera.

The Nautilus 19: 63-67, pi. 2.

Richardson, L. 1985. Camaenidae: Catalog of species. Tryonia

12: 1-479.

Schileyko, A. A. 2003. Treatise on recent terrestrial pulmonate

mollusks. Trigonochlamydidae, Papillodesmidae, Vitri-

nidae, Limacidae, Bielziidae, Agriolimacidae, Boetgeri-

llidae, Camaenidae. Ruthenica, Supplement 2. Part 11:

1467-1626.

Yen. T. -C. 1939. Die chinesischen land- und SiiBwasser-Gas-

tropoden des Natur- Museums Senckenberg. Abhandlun-

gen der Senckenbergisch-Naturforschenden Gesellschaft

444: 1-234, Tafel 1-16.

Zilch, A. 1959-1960. Gastropoda, Euthyneura. In: Handbuch

der Paliiozoologie (O. H. Sehindewolf, ed.), 6: 1-834.

Gebriider Borntraeger, Berlin.

Zilch, A. 1966. Die typen und typoide des Natur-Museum

Senckenberge, 34: Mollusca: Camaenidae (4). Arehiv ftir

Molluskenkunde 95: 197-223.

THE NAUTILUS 124(1 ):25-33, 2010

Page 25

Terrestrial gastropods from Haida Gwaii (Queen Charlotte

Islands), British Columbia, Canada, including description

of a new northern endemic slug (Gastropoda:

Stylommatophora: Arionidae)

Rristiina Ovaska

Biolinx Environmental Research Ltd.

424 Viaduct Avenue, Victoria

V9E 2B7, CANADA

[email protected]

Lyle Chichester

209 Chestnut Springs Way,

Williamston SC 29696 USA

[email protected]

Lennart Sopuck

Biolinx Environmental Research Ltd.

1759 Colburne Place, Sidney

BC VSL 5A2, CANADA

[email protected]

ABSTRACT

Reflecting its isolation, geography, and glacial history, the

Haida Gwaii archipelago (Queen Charlotte Islands, British

Columbia) contains numerous endemic and disjunct taxa of

various groups of organisms, but terrestrial gastropods have

received scant attention. During surveys of 56 sites on Graham

and Moresby Islands and 11 smaller islands, including remote

mountain top locations, we detected 18 species of native ter-

restrial gastropods, most of which also occur in southwestern

British Columbia. An undescribed species of semi-slug was

found at four sites on Graham Island and six sites on Moresby

Island and is formally described (Arionidae: Staala gwaii).

Morphological and anatomical analyses suggest that the new

slug is related to small species of Hemphillia Bland and Binney,

1872, but the differences are substantial, warranting the estab-

lishment of a new genus. The new species is of particular

interest because it appears to be a northern endemic and a

relict to the archipelago.

Additional keywords: Gastropoda, Arionidae, Staala gwaii ,

Queen Charlotte Islands, anatomy, endemism

INTRODUCTION

Haida Gwaii (Queen Charlotte Islands) is an isolated

archipelago located at the edge of the North American

continental shelf in the North Pacific Ocean. A distance

of at least 80 km separates the islands from the nearest

landmass to the east across Hecate Strait on the mainland

British Columbia and to the north across Dixon Entrance

on the Alaskan panhandle. The biota of the islands in-

cludes endemic and unusual disjunct populations from a

wide range of taxonomic groups (e.g., vascular plants:

Ogilvie, 1989, 1994; bryophytes: Schofield, 1989a,b; cara-

bid beetles: Clarke et al., 2001; birds and mammals:

McTaggart Cowan, 1989). Endemism and disjunct distri-

butions have been interpreted to reflect the geographic

isolation of the archipelago and differentiation in situ , in

combination with complex patterns of past recolonization

and extinction events.

Terrestrial gastropods of Haida Gwaii are poorly

documented, and knowledge of this group is largely

restricted to serendipitous observations as part of studies

of other organisms. Terrestrial gastropods as a group can

be useful for elucidating phylogeographic patterns, as

many species have poor dispersal abilities it not aided

by humans and can survive in small habitat patches

(Cowie and Holland, 2006). From 2000 to 2004, we sur-

veyed numerous sites on the two main islands (Graham

and Moresby) and on smaller islands of the archipelago

for terrestrial gastropods. Here we report the results of

these surveys and describe a new genus and species of

arionid semi-slug, presumed to be a relict, and endemic

to the archipelago.

MATERIALS AND METHODS

Study Sites; We sampled 56 sites on Graham (6883

km") and Moresby (3066 km") islands and on 1 1 smaller

islands in the Hecate Strait: Lyell (181 km"), Kunghit

(134 km2), Burnaby (66 km"), Tanu (23 km"), Huxley

(6.7 km2), SGang Gwaii (2.9 lori2), Kat (0.7 km2), Bischofs

(1.1 km"), Hotspring (0.2 km"), Ellen (0.2 km"), and

Slug Islet (0.03 km") (Figure 1; see RBCM website

for coordinates and habitat descriptions). More than one

habitat or sub-site within a 1 km area was sampled at

seven of these sites. The surveys took place in Apr. 2000,

Jul.-Oct. 2002, Sep.-Nov. 2003, and Sep. 2004. The focus

was on old-growth forest (28 sites), dominated by Picea

sitchensis, Tsuga heterophylla , and Thuja plicata and

with an understory of Vaccinium species, Gaultheria

shallon, Menziesia ferruginea , and Blechnum spirant.

Other habitats sampled consisted of older (> 80 years

old) second-growth coniferous forest (12 sites), young

forest with a large component of Abuts rugosa (< 60 years

old) (3 sites), subalpine and alpine meadows (7 sites), bog

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THE NAUTILUS, Vol. 124, No. 1

Figure 1. Map of sampling sites in the Haida Gwaii (Queen

Charlotte Islands archipelago. Site numbers correspond to those

in Table 1 (see RBCM website for coordinates and habitats).

Biogeoclimatic zones: AT-alpine tundra, MH-mountain hemlock,

CWH-coastal western hemlock (Meidinger and Pojar, 1991).

with stunted trees (3 sites), and other open habitats (rocky

bluff, wet meadow, riparian fringe, thermal meadow, sand

dune) (9 sites). The alpine sites were on rocky slopes with

sparse ground cover, including hummocks ol grasses,

sedges, heathers, and erowberry ( Empetrum nigrum).

The subalpine sites contained scattered stunted trees

and shrubs, including Pinus contorta , Chamaecyparis

nootkatensis , Tsuga mertensiana , and Juniperus species.

In 2004, we specifically targeted subalpine-alpine habi-

tats, which were suspected to support populations of the

new species of slug.

Gastropod Sampling and Identification: The main

survey methods consisted of timed searches of natural

cover on the forest floor (59 plots at 50 sites) and inspec-

tions of cardboard cover-objects (36 plots at 9 sites).

Additionally, we extracted small snails from litter sam-

ples from two sites, including an experimental forestry

site that was sampled intensively in two years (102 1 of

litter dried and sieved and residues examined for snail

shells). Searches of natural cover focused on key micro-

habitat features for gastropods, such as piles of bark or

an abundance of decaying logs or stumps. Observers

visually scanned the surface of the forest floor and vege-

tation, turned over downed logs, sloughed-off bark, and

rocks, and examined handfuls of leaf-litter. At one site

(Site 2a-d in Figure 1), the surveys were both time- and

area-constrained, and the observers searched 100x1 m

transects in four different habitats for 40 minutes. The

total search time for surveys of natural cover was 86.7

person-hours (x ± SE = 88 ± 7 min/site).

The cardboard cover-object method (Hawkins et ah,

1998) permitted repeated sampling of gastropods with

minimal disturbance to the habitat. We used cover-

objects constructed of layers of corrugated cardboard

(dimensions 30 cm x 30 cm) placed at stations 10 m apart

along transects of 10 sampling stations and inspected

them one or more times after they had weadiered on the

forest floor for at least two weeks. There were a total of

1072 cardboard cover-objects on 36 plots at 9 sites. One

site (Site 1 in Figure 1) was used as an experimental site

for investigating logging effects and was sampled inten-

sively and repeatedly (800 cover-objects inspected four

times; in 2002 anti 2006; KO and LS, unpublished data).

Identification of gastropods was based on descriptions

in Pilsbry (1940, 1948) and Forsyth (2004). Nomencla-

ture follows Forsyth (2004). Snails were identified using

shell characteristics. Any small snails that could not be

readily identified in the field were collected and exam-

ined under a dissecting microscope. Some snails (notably

juveniles of Ancotrema and Pristiloma , and most Vertigo)

were identified to genus only. Of slugs, several spec-

imens of Staala gwaii , new species, and a sample of

Prophysaon foliolatum, and P. vanattae, were dissected,

and their reproductive anatomy was examined. Voucher

specimens are deposited in the Royal British Columbia

Museum, Victoria, British Columbia, Carnegie Museum

of Natural History, and in the personal collections of

K. Ovaska and R. Forsyth.

Dissection of Specimens: Seven specimens of the

new species, preserved in 70% ethanol, were dissected

by LC under a dissecting microscope (7.5-35X magnifi-

cation). Parts removed for further study were mounted

on standard microscope slides and examined under a

compound microscope (40-400X magnification). Hema-

toxylin stain was used to make a permanent slide of the

penis. Mounted specimens were dehydrated in 95%

and 100% ethanol. Toluene was used as a clearing agent

and specimens were mounted in Permount (Fisher Sci-

entific, Fairlawn, New Jersey).

RESULTS

Gastropod Species Found

Surveys of 56 sites resulted in the detection of 18 native

and four alien species of terrestrial gastropods (Table 1).

Five species predominated in the samples: Ariolimax

columbianus (71.4% of sites), Vespericola columbianus

sp. (subgenus Pristiloma)

Polygyridae:

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THE NAUTILUS, Vol. 124, No. 1

(71.4% of sites), Prophysaon foliolatum ( 60.7 % of

sites), Haplotrema vancouverense (66.1% of sites), and

Pristiloma stearnsii (57.1% of sites). All these species

were widely distributed in forests throughout the archi-

pelago. Several snails with unusual, clear, transparent

shells were found at one locality on Graham Island (Site

1 in Figure 1), but were attributed to Pristiloma stearnsii

based on other shell features.

We found IS species of terrestrial gastropods on

Graham Island and 15 on Moresby Island. On the

smallest island sampled, a rocky bluff (Slug Islet), we

found two species; on the remaining 10 small islands

we found 4-9 species each (x = 6.4, SD = 1.6).

Alien gastropods, represented by four species, were

found only at a few sites that were either disturbed and

in early suecessional stages on Graham and Moresby

Islands or received regular human visitation (Hotspring

Island); older forest and small islands, apart from

Hotspring Island, appeared to be free of alien species.

Slugs, represented by P. foliolatum , P. vanattae, and

S. gwaii , dominated the gastropod fauna in the subal-

pine and alpine sites sampled, whereas other gastro-

pods, including A. columbianus, H. vancouverense , and

P. stearnsii were found infrequently and in very low

numbers in these habitats; A. columbianus occurred only

at sites with patches of trees and shrubs. P. foliolatum was

the only gastropod found at two alpine sites that were

devoid of trees and shrubs (Sites 31 and 34 in Figurel).

A New Species of Arionid Slug

A slug that did not fit within the description of any known

species was encountered at four sites on Graham Island

and six sites on Moresby Island (Figure 2, 3). The locali-

ties were near Rennell Sound, south of Port Clements,

and on Alt. Genevieve (Sleeping Beauty Massif) on Gra-

ham Island, and on Yatza Mountain, Ml. Oliver, Mt. De la

Touche, unnamed mountains near Sunday Inlet and

Kostan Inlet, and in Louscoone Inlet on Moresby Island.

Superficially, the slug resembled Hemphillia glanclulosa

Bland and W.G. Binney, 1872, found on Vancouver Island,

British Columbia, and in Washington and Oregon, but

detailed morphological and anatomical examination re-

vealed substantial differences, warranting the establish-

ment ol a new genus. Preliminary genetic analyses using

mitochondrial markers also place the species apart from

all known genera of arionid slugs in western North Amer-

ica (Clade C in Wilke, 2004: fig. 2).

Arionid genera native to the Pacific Northwest include

Zacoleus Pilsbry, 1903, Udosarx Webb, 1954, Prophysaon

Bland and W.G. Binney 1873, Kootenaia Leonard,

Chichester and Baugh, 2003, and Hemphillia Bland and

W.G. Binney 1872. Arionid genera share a ribbed jaw.

The new slug possesses a jaw that is subdivided into

sectors by evenly spaced, finely incised lines. We con-

sider this jaw to be sufficiently similar to the jaws ol other

arionids to warrant the inclusion ol the new species to

this family. The new slug further differs from the first

four genera by possessing a visceral cavity that is elevated

Figures 2-3. Staala gwaii. 2. Adult (17 mm in extended

length) from near Port Clements, Graham Island (Type locality.

Site 1 in Figure 1). 3. Juvenile (2 mm in extended length) from

near Port Clements, Graham Island (Type locality. Site 1 in

Figure 1).

into a hump and that fails to extend to the tip of the tail.

It shares this character with Hemphillia (jumping-slugs),

the only other genus of native semi-slugs known from

North America. It differs from Hemphillia by having a

shell plate that is calcareous and completely covered by

the mantle and by a pattern of papillae covering the

entire body. See Table 2 for comparisons of major fea-

tures among western North American genera of arionids.

A formal description of the new genus, Staala, and spe-

cies, S. gwaii, follows.

Staala new genus

Type Species: Staala givaii new species (below).

Diagnosis: Distinct from any other known arionid

genus externally by having viscera in a pronounced

hump and shell covered by mantle, and internally by the

complexity of the penial stimulatory apparatus (see de-

scription in the following species account) and by the

presence of an atrial accessory sac.

Etymology: The generic name means “slug” in Haida

language and honors the aboriginal heritage of the archi-

o o o o

pelago of Haida Gwaii (Queen Charlotte Islands).

K. Ovaska et al., 2010

Page 29

Table 2. Comparison of external and internal characteristics of Staala (new genus) with those of five other genera of Arionidae

native to western North America.

*Except the main branch of the left tentacular retractor, which originates on the floor of the body cavity.

Staala gioaii new species

Description: Size: Veiy small; length of 16 live spec-

imens was 2-17 mm (x = 9.8 mm, SD = 5.7 mm) when

extended in movement. Length of 12 preserved specimens

was 3- 11 mm (x= 8.1 mm, SD = 2.7 mm); the difference in

size between live and preserved specimens probably

reflects preservation techniques (live animals were maxi-

mally extended whereas the preservative, ethanol, resulted

in shrinkage). Holotype: 16 mm live, 9.4 mm preserved.

Smallest dissected and preserved individuals with a mature

reproductive system were 8 mm in length.

External Anatomy: The following description is based on

examination of 40 individuals from ten sites and apply to

the holotype, unless otherwise mentioned. Shell dome-

shaped and completely covered by mantle. Outer layer

horny and thin, and covering the entire visceral hump;

inner layer calcareous, thickest at the center of the dome

and largely absent at the margins. Mantle elliptical and

large, about 2/3 the length of the body and covering the

visceral pouch, which is elevated into a pronounced

hump; mantle hump flattened dorsally towards its distal

end and can be slightly asymmetrical, giving it a mis-

shapen appearance. Pneumostome slightly anterior or in

the middle of the right side of the mantle, near mantle

margin. Tail rounded dorsally, no keel evident; tail flat-

tened and depressed at its base where the distal portion

of the mantle rests. Several elevated lines of papillae and

associated grooves radiate outwards from the depression.

Tail protrudes distally over foot. Caudal mucus pore pre-

sent. Head, mantle, and tail covered with numerous papil-

lae. Foot fringe moderately wide; sole undivided.

Color: Head and base of tentacles dark grey, sometimes

bluish; tentacles lighter grey towards tips. Mantle mot-

tled with dark grey and light grey (as in holotype) or tan,

sometimes flecked with small tan specks. Dorsal surface

of head and tail dark grey. Foot fringe light grey or tan.

lighter than sides, sometimes with indistinct dark, verti-

cal lines. Underside of head similarly light grey or tan.

Black-tipped papillae often form dotted line at foot mar-

gin. Sole light grey or tan, dark grey in some melanistic

individuals. Papillae covering head, mantle, and tail are

light grey and black-tipped. Individuals from some local-

ities, especially subalpine habitats on Moresby Island,

were melanistic and almost uniformity dark with the

exception of the sole that is slightly lighter.

Internal Anatomy: Reproductive System: The ovo-

testis comprises a large number of lobules (more than

three dozen). It is partially embedded on the right pos-

terior of the digestive gland. The exposed portion is

lightly to moderately pigmented with black flecks. The

hermaphroditic duct is long, slender, and straight in

immature individuals and swollen and highly convoluted

in sexually mature animals. The albumen gland is adher-

ent to the spermoviduct (common duct). In sexually

mature individuals both the albumen gland and the

spermoviduct become greatly enlarged and the latter

becomes structurally more elaborate. In most individuals

the spermathecal duct and tree oviduct enter the shallow

atrium separately. In two sexually immature individuals

the two ducts joined just before entering the atrium. The

spermatheca (seminal receptacle or bursa copulatrix) is

conical to ovoidal in shape; its duct is slender and

tapered. In one specimen containing a single spermato-

phore, the spermatheca was forced into a fusiform shape

and its duct into a corkscrew. The vas deferens arises as a

slender duct from the spermoviduct, which also gives

rise to the free oviduct. The vas deferens becomes even

more slender as it curves around the base of the penis at

the penial junction with the atrium, only to thicken again

as it transitions along the side of the penis eventually to

become a greatly thickened epiphallus (Figure 4).

The epiphallus enters the penis at its apex. Inserted at

the apex, at this epiphallus-penis junction, is the penis

THE NAUTILUS, Vol. 124, No. 1

Page 30

Figures 4-6. Reproductive anatomy of Staala g waii (specimen from type locality). 4. Reproductive system. 5. Bisected penis of

two specimens of Staala g waii from the type locality. Left: upper verge chamber (empty) and lower stimulatory chamber with its

complex folds and lobes. Scale bar = 0.2 mm; Right: bisected verge in the upper chamber and a portion of the stimulator in the lower

chamber. 6. Spermatophore (ca. 2 mm in length) showing the denticle region (arrow). Terminal portion of the filament is missing.

Abbreviations: A, atrium; AG, albumen gland; AS, accessory 'sac: EP, epiphallus; FO, free oviduct; HD, hermaphroditic duct; OT,

ovotestis; P, penis; PR, penis retractor muscle; SP, spermatheca (bursa copulatrix); S, stimulator; SPD, spermathecal duct; SPOV,

spermoviduct; V, verge; VD, vas deferens.

retractor muscle, which is a wide band that passes

directly back to its origin near the midline of the dia-

phragm. The penis is a large barrel-shaped structure

divided internally into an upper verge chamber and

a lower stimulator chamber (Figures 4, 5). A lightly

pigmented band on the penis surface roughly cor-

responds to the boundary between the two inner

chambers. The verge chamber contains a large conical

structure we believe functions as a verge. The lumen

of the epiphallus continues within the verge as a narrow

passage that opens at or near the apex of the cone. The

lower stimulator chamber is almost completely filled

with a variety of attachments on the inner penial wall.

Some are plumose while others are smooth-margined

and lobed. In other slug species such structures have

been referred to as stimulators and we extend that tra-

dition in this case, although we have not been able to

observe copulation to determine how this complex is

employed. The penis enters the atrium independent

of the spermathecal duct and the free oviduct. There is

no accessory penial sac. However, there is a small atrial

accessory sac present. This sac has a very slender duct,

which enters the atrium independent of the other ducts.

In immature individuals the sac is very small and difficult

to see. A single spermatophore was found intact in one

specimen. The spermatophore consists of a crescent-

shaped main body and a long threadlike terminus

(Figure 6). Near the junction of the two parts the surface

bears a number of tiny denticles. Tbe overall length of

the spermatophore is about 2 mm.

Buccal and Tentacular Retractor Muscles: The left

and right buccal retractor muscles fuse just posterior of

the buccal mass. The fused band passes directly back to

the origin near the midline of the diaphragm. The right

tentacular retractor muscle passes between the male and

female components of the reproductive system to its

origin near the midline of the diaphragm. The left ten-

tacular retractor muscle is split into a main branch that

originates from the floor of the body cavity on the left

side. The other branch is very slender, almost nerve-like.

This branch extends backward toward an origin near the

midline of the diaphragm thus preserving an overall pat-

tern one might describe as converging. This pattern is

disrupted only by the anomalous branch of the left ten-

tacular retractor. We did not find a retensor muscle.

Digestive System: The jaw bears line, evenly spaced

incised lines but is not ribbed. Tbe radula is of the

usual arionid type, with the central row of teeth tricus-

pid, the inner lateral rows bicuspid and the outer rows

K. Ovaska et al., 2010

Page 31

tending toward elongation of the mesocones and reduc-

tion of the eetoeones. The crop is large but otherwise

unremarkable. The short, slender intestine makes three

looping turns before arriving at the anal pore.

Holotype: From type locality, on cardboard cover-

objects used to sample gastropods in a coniferous stand

of mixed old-growth and naturally regenerated mature

second-growth forest at elevation of 65-80 m; collected

by J. Gray, L. Hyatt, C. Engelstoft, 7 Oct. 2002, Royal

British Columbia Museum, RBCM 009-00035-001.

Paratypes: (1) Near summit of Mt. Genevieve, Gra-

ham Island (53°33.9' N, 132°5.6/ W), from cardboard

cover-objects in alpine meadow at elevation of about

800 nr; collected by Luke Hyatt, 16 Oct. 2002, RBCM

009-00036-001; (2) mid-slope of Mt. Genevieve

(Sleeping Beauty Trail; 53°15.8/ N, 132°12.9' W), from

cardboard cover-objects in old-growth coniferous forest

at elevation of 340 m, collected by Kristiina Ovaska,

Lennart Sopuek, and Bern Wijdeven, 22 Sep. 2004,

Carnegie Museum of Natural History, CM97971 and

RBCM 009-00038-001 .

Type Locality: 13 km southeast of Port Clements,

Graham Island (53°34.6' N, 132°6.6/ W), Queen Char-

lotte Islands, British Columbia, Canada; a coniferous

stand of mixed old-growth and naturally regenerated

mature second-growth forest at elevation of 65-80 nr.

Other Material Examined: Collected from Moresby

Island by Kristiina Ovaska and Lennart Sopuek from

under rocks or within krummholtz hummocks in subalpine

meadows: (1) Yatza Mountain (52°21,5' N, 13F26.0' W),

elevation 170-210 m, 14 Sep. 2003, RBCM 009-00037-

001; (2) Mt. Oliver (52° 42.9' N, 132°1.4' W), elevation

650 m, 14 Sep. 2004, RBCM 009-00039-001; (3) unnamed

mountain near Kostan Inlet (52°34.7' N, 131°44.0' W),

elevation 280 m, 14 Sep. 2004, RBCM 009-00041-001;

(4) unnamed mountain near Sunday Inlet (52°37.9' N,

131°50.4' W), elevation 475 m, 14 Sep. 2004, RBCM

009-00040-001; (5) from within leaf litter along bank of

small stream in old-growth coniferous forest: Louscoone

Inlet (52° 10.0' N, 131° 12.7' W), elevation < 50 m, 17 Sep.

2004; RBCM 009-00042-001.

Etymology: The specific name (used as a name in

apposition) g waii means “island” or “home” in the Haida

language and refers to the archipelago the slugs inhabit.

Natural History: The ten sites where the species was

found ranged from lowland coniferous forest, dominated

by Sitka spruce ( Picea sitchensis ), western redeedar (Thuja

plicata ), and western hemlock (Tsuga heterophylla), to sub-

alpine tundra. The species was seldom found in lowland

forest (2 sites), although most extensive search effort was

in this habitat. It was more frequently encountered at mid-

elevation forest containing yellow cedar ( Chamaecyparis

nootkatensis), mountain hemlock (Tsuga mertensiana),

and/or shore pine ( Pinus contorta), and in subalpine

meadows and mountain slopes. The subalpine habitats

were very moist with scattered, stunted (< 2 m tall) trees

and bushes (P. contort a, C. nootkatensis, T. mertensiana ,

and Juniperus sp.) and swales of grasses, heather, and crow-

berrv (Empetnim nigrum). In these habitats, we found

slugs under rocks or within hummocks of ground vegeta-

tion. At the forested sites, we located the species by using

cardboard cover-objects (see Methods); only one individual

was found during visual searches of the forest floor. We

found the smallest juveniles, about 2 mm in extended

length, on 27-28 Jul. and 26 Sep. 2002 at a lowland site

(Site 1 in Ligure 1). We found larger juveniles and adult-

sized individuals (> 10 mm in extended length) from Sep-

tember to November, 2002-2004. Longevity and life stages

at which the slugs survive winter are unknown.

Possible Taxonomic Relationships: Of the previ-

ously described species, the new species most closely

resembles small species of HemphiUia (PI. glandulosa/

PI. hurringtoni species complex). It differs from them

externally by a mantle that completely covers the shell

plate, which in the new species is calcareous, by dense,

pointed papillae that cover the sides and the tail as well

as the mantle, and by an unkeeled tail, and internally by

an unusual configuration of buccal and tentacular retrac-

tors (Table 2).

DISCUSSION

The terrestrial gastropod fauna of Haida Gwaii is depau-

perate when compared to more southern areas along the

Pacific coast, probably reflecting the isolation and harsh,

northern climate of the archipelago; 18 native species

were detected in contrast to over 35 species on Vancou-

ver Island (Lorsyth, 2004). With the notable exception of

the new slug, Staala gwaii, all species of gastropods

found during the surveys also occur on Vancouver Island

and the coastal mainland of southern British Columbia.

However, systematic relationships of some groups such

as Prophysaon, Pristiloma , and Vertigo from western

North America have not been examined recently, and

genetic or detailed morphological studies could reveal

differences among populations from Haida Gwaii and

farther south. In particular, the unusual, clear-shelled

Pristiloma, attributed herein to P. stearnsii, requires fur-

ther investigation.

Curiously, we detected only infrequently two species

that are relatively common on Vancouver Island and

the lower mainland of British Columbia, Nesovitrea

binneyana and Euconulus fulvus. Both snails were

present in thermal meadows on Hotspring Island;

N. binneyana also occupied sand dune habitat near

Masset, Graham Island. We encountered Cryptomastix

germana at only two sites within pockets of dense ri-

parian herbaceous vegetation. This species has been

reported previously from one Moresby Island locality

(Lorsyth, 2000). Some species (Planogyra clappi,

Cryptomastix germana) probably exist at or near their

northern limits of distribution in Haida Gwaii.

THE NAUTILUS, Vol. 124, No. 1

Page 32

The new species of slug is of particular interest

because it is possibly a relic of an ancient lineage that

has survived several periods of glaciation on the archi-

pelago. Ice-free refugia existed in various locations

along the North Pacific coast from the Aleutian Islands

to Vancouver Island during Pleistocene glaciations,

and such refugia could have permitted the persistence

of this and other endemic and disjunct species known

from the islands through tins and earlier glacial epi-

sodes. Paleoeeological evidence exists for lowland

ice-free refugia in Haida Gwaii at the height of the

Wisconsin glacial epoch (Warner et ah, 1982), but a

continuous record of micro- or macro-fossils through

this period is lacking. Some mountain tops in the Queen

Charlotte Range are also thought to have remained as

ice-free nunataks throughout glacial periods (Heusser,

1989) and probably supported organisms such as bryo-

pliytes (Schofield, 1989a) that are able to exist in

small microhabitats and withstand harsh conditions.

The slug could conceivably also have persisted in nuna-

taks, as it is presently found in isolated mountain top

habitats.

Some endemics on the archipelago appear to be of

relatively recent origin as a result of rapid morphological

evolution in post-glacial times within the past 15,000-

16,000 years (e.g., carabid beetles of the genus Nebria:

Clarke et ah, 2001; Haida Gwaii black bear, Ursus

americmms carlottae: Byun et ah, 1997), whereas others

are thought to be much older. Ancient, possibly Tertiary

origins have been postulated for relic species of bryo-

phytes that show unusual, disjunct distribution patterns

(Schofield, 1989a).

Preliminary molecular analyses suggest that the line-

age containing Staala gwaii is old and has split from

Hemphillia , the presumed sister taxon, several million

years ago (Wilke, 2004; Thomas Wilke, Animal Ecology &

Systematic^, Justus Liebig University Giessen, Giessen,

Germany, pers. comm.), lending support to the notion

that the slugs survived several glacial periods in refugia

on the islands or elsewhere along the northwest coast of

North America. Several species of plants endemic to the

northwest coast have scattered and disjunct distributions

(Calder and Taylor, 1968; Taylor, 1989; Ogilvie, 1989).

Examples of endemic plants that co-occur with the slug

in subalpine habitats in Haida Gwaii include Geum

schofieldii , Ligusticum calderi , Saxifraxa taylori , and

Senecio moresbiensis on Mt. De la Touche; Ligusticum

calderi and Saxifraga taylori on Mt. Yatza; Ligusticum

calderi on Mt. Oliver; Saxifraga taylori and Senecio

moresbiensis on an unnamed mountain east of Blue

Heron Bay (plant distribution from unpublished data

files by Parks Canada).

Further surveys along the northwest coast of main-

land British Columbia are needed to document the

extent of the distribution of Staala gwaii and to ex-

plore the existence of other undiscovered species and

populations. Comparative studies with other western

North American and northeast Asian forms are also

desirable, as they have potential to shed light on the

evolution and biogeography of western North American

slugs.

ACKNOWLEDGMENTS

We thank Glen Dunsworth, Bill Beese, Brian Reader,

Scott Parker, Barb Johnston, and Arthur Robinson for

their support of the project and help with logistics. Tom

Wilke accepted specimens for genetic analysis and

shared with us his unpublished data. Luke Hyatt, Janet

Gray, Berry Wijdeven, and Christian Engelstoft assisted

in the field. Richard Lamy and Debbie Gardiner acted

as our guides in Gwaii Haanas. Kelly Sendall and

Moretta Frederich, and Tim Pearce accepted specimens

for the collections at Royal British Columbia Museum

and Carnegie Museum of Natural History, respectively.

Alvin Cober prepared the base-map for Figure 1 . Robert

Forsyth, Tim Pearce, and an anonymous reviewer

provided helpful review comments. Funding from

Weyerhaeuser Canada, Western Forest Products, En-

dangered Species Recovery Fund (Environment Canada

and World Wildlife Fund), Wildlife Habitat Canada,

Department of National Defence, and Parks Canada for

Biolinx Environmental Research Ltd. made fieldwork in

Haida Gwaii possible.

LITERATURE CITED

Byun, S. A., B.F. Koop, and T. E. Reimchen. 1997. North Amer-

ican black bear mtDNA phylogeography: Implications for

moqrhology and the Haida Gwaii glacial refugium contro-

versy. Evolution 51: 1647-1653.

Clarke, T. E., D.B. Levin, D.H. Kavanaugh, and T. E.

Reimchen. 2001. Rapid evolution in the Nebria gregaria

group (Coleoptera: Carabidae) and the paleogeography of

the Queen Charlotte Islands. Evolution 55: 1408-1418.

Calder, J.A. and R.L. Taylor. 1968. Flora of the Queen Char-

lotte Islands. Part 1. Systematics of the vascular plants.

Canada Department of Agriculture Monograph 4.

Queen's Printer, Ottawa, Ontario, Canada, xiii + 659 pp.

Cowie, R.PI. and B.S. Holland. 2006. Dispersal is fundamental

to biogeography and the evolution of biodiversity on oce-

anic islands. Journal of Biogeography 33: 193-198.

Forsyth, R.G. 2000. The land snail Cryptomastix german a

(Gastropoda: Polygyridae) in the Queen Charlotte Islands,

British Columbia: a range extension north from Vancouver

Island. Canadian Field-Naturalist 114: 316-317.

Forsyth, R.G. 2004. Land snails of British Columbia. Royal

British Columbia Museum handbook. Royal BC Museum,

Victoria, British Columbia, Canada. 188 pp.

Heusser, C.J. 1989. North Pacific coastal refugia - the Queen

Charlotte Islands in perspective. In: Scudder, G.G.E. and

N. Gessler (eds). The Outer Shores of Queen Charlotte

Islands. Queen Charlotte Islands Museum Press,

Skidegate, British Columbia, pp. 91-106.

Hawkins, J.W., M.W. Lankester, and R.R.A. Nelson. 1998.

Sampling terrestrial gastropods using cardboard sheets.

Malacologia 39: 1-9.

McTaggart Cowan, 1. 1989. Birds and mammals on the Queen

Charlotte Islands. In: Scudder, G.G.E. and N. Gessler

(eds). The Outer Shores of Queen Charlotte Islands.

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Queen Charlotte Islands Museum Press, Skidegate, Brit-

ish Columbia, pp. 175-186.

Ogilvie, R.T. 1989. Disjunct vascular flora of northwestern

Vancouver Island in relation to Queen Charlotte Islands’

endemisms and Pacific coast refugia. In: Scudder, G.G.E.

and N. Gessler (eds). The Outer Shores of Queen Char-

lotte Islands. Queen Charlotte Islands Museum Press,

Skidegate, British Columbia, pp. 127-130.

Ogilvie, R.T. 1994. Rare and endemic vascular plants of

Gwaii Ilaanas (South Moresby) Park, Queen Charlotte

Islands, British Columbia. British Columbia Ministry of

Forests, Forest Science Program. FRDA Report 214

(available online at http://www.for.gov.bc.ca/hfd/pubs/

Docs/F rr/F rr2 1 4.htm )

Pilsbry, II. A. 1940. Land Mollusca of North America (north of

Mexico). The Academy of Natural Sciences of Philadel-

phia, Monograph 3, VI, Part 2: 575-994, i-ix.

Pilsbry, H.A. 1948. Land Mollusca of North America (north of

Mexico). The Academy of Natural Sciences of Philadel-

phia, Monograph 3, V2, Part 2: i-xlvii, 521-1113.

RBCM (Royal British Columbia Museum, Victoria, B.C.)

website. http://www.royalbcmuseum.bc.ca/Content_Files/

Files/Collections%20and%20Research/Natural%20History/

Haida_Gwaii_gastropod_survey_sites.pdf

Schofield, W. B. 1989a. Structure and affinities of the bryoflora

of the Queen Charlotte Islands. In: Scudder, G.G.F. and

N. Gessler (eds). The Outer Shores ol Queen Charlotte

Islands. Queen Charlotte Islands Museum Press, Skidegate,

British Columbia, pp. 109-119.

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Hemisphere: Europe and North America. Botanical Jour-

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Taylor, R.L. Vascular plants ol the Queen Charlotte Islands.

1989. In: Scudder, G.G.E. and N. Gessler (eds). The

Outer Shores of Queen Charlotte Islands. Queen Char-

lotte Islands Museum Press, Skidegate, British Columbia,

Canada, pp. 121-125.

Warner, B.G., R.W. Mathewes, and J.J. Clague. 1982. Ice-free

conditions on the Queen Charlotte Islands, British Colum-

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THE NAUTILUS 124(1 ):34-40, 2010

Page 34

How the number of hinge teeth may induce errors in the

taxonomy of Nuculidae and Nuculanidae (Bivalvia)

Cleo Dilnei de Castro Oliveira

Tatiana Huguenin Morales

Departamento de Zoologia, Instituto de Biologia

Universidade Federal do Rio de Janeiro, 1 1 ha do Fundao

21941-590

Rio de Janeiro, BRAZIL

[email protected]

ABSTRACT

The hinge figures as an important feature in the taxonomy of

bivalves, especially when soft parts are not available. For the

Protobranchia, in addition to other shell features, the number

of hinge teeth is often used in taxonomic studies. However,

despite the importance of the number of hinge teeth, this char-

acter is not informative when shell size measurements are not

available, since the number of teeth can increase during ontog-

eny. In addition, intraspecific variation may be observed for the

same shell-size class. Since this variation has been up to now

only empirically observed, the present study provides a statisti-

cal approach to the problem by computing the linear regression

between number of teeth and shell size in 310 valves from five

protobranch species (family Nuculidae: Pronucula benguelana;

Nucula semiomata ; Ennucula puelcha-, and family Nuculani-

dae: Adrana electa ; A. patagonica.) All species showed a statis-

tically significant relationship (P value < 0.0001) between these

characters.

Additional Keywords: Linear regression, shell morphology,

Nuculoidea, Nuculanoidea, Protobranchia, taxonomy

INTRODUCTION

The protobranchs are a dominant bivalve group at abys-

sal depths, encompassing a high percentage of the bi-

valve species found in the deep-sea (Sanders and Allen,

1973). The recent sampling of deep-sea benthic fauna

and the efforts of many investigators (e.g. Allen and

Sanders, 1973, 1996; Moore, 1977; Rhind and Allen,

1992; Kilburn, 1994, 1999; Gofas and Salas, 1996; Roy

et al., 2000; Allen, 2008; La Perna, 2008) have increased

the number of known species and enlarged the known

ranges of many protobranchs, providing a source for

different proposals of classification for the group (e.g.

Poel, 1955; Purchon, 1959; Cox, I960; McAlester, 1964;

Newell, 1969; Verril and Bush, 1897; Yonge, 1959;

Sanders and Allen, 1973; Scarlato and Starobogatov,

1985; Allen and Hannah, 1986; Maxwell, 1988; Morton,

1996; Salvini-Plawen and Steiner, 1996; Coan, Scott, and

Bernard, 2000; Schneider, 2001; Giribet and Wheeler,

2002; Giribet, 2008).

Among the protobranchs, the Nuculoidea Gray, 1824,

and Nuculanoidea Adams and Adams, 1858, have had a

problematic taxonomic history, often with obscure rear-

rangements of species and unclear changes in the

higher-level taxonomy of many names (for more details

see Sehenck, 1934; Poel, 1955; Allen and Hannah, 1986;

Maxwell, 1988; Rhind and Allen, 1992; Zardus, 2002).

Most of the difficulties involved in the classification of

the group arise from the conservative nature of the shell

shape (Allen and Hannah, 1986) and from the morphol-

ogical approach, which often considers only a single set

of features (Sanders and Allen, 1973).

Although several characters have been taken into

account (e.g., general outline, ornamentation and micro-

structure of the shell), in most taxonomic descriptions of

protobranchs the hinge usually is an important taxonom-

ic feature, especially when the studied specimens lack

soft parts. The shape, number, position, and spacing of

the teeth are often used in the diagnoses of species and

even genera (Dali, 1886; Gofas and Salas, 1996). More-

over, the differences between the number of anterior

and posterior teeth are used in identification, and even

differences in the order of two or three teeth have been

considered significant in descriptions or identification

works (e.g. Esteves, 1984; Smith, 1885; Abbott, 1974;

Kilburn, 1994; Rios, 1994; Espinosa and Ortea, 2001).

However, to consider the number of teeth without

associating the character to measurements of shell size

is not informative, and may cause taxonomic confusion.

A morphometrieal approach may improve on the tradi-

tional taxonomic methods and has been used with suc-

cess by several authors (Bonfitto and Sabelli, 1995;

Gofas and Salas, 1996; Fuiman et ah, 1999).

This paper discusses the taxonomic importance of the

size of the shell in proportion to the number of teeth on

the hinge in three species of Nuculidae: Pronucula ben-

guelana Clarke, 1961; Nucula semiomata d’Orbigny,

C.D.C. Oliveira and T.H. Morales, 2010

Page 35

VENTRAL

POSTERIOR

Figure 1. Ennticula puelclio d’Orbigny, 1S42. Shell and the anterior and posterior hinge teeth. Abbreviations: at = anterior teeth;

pt = posterior teeth. Scale bar = 2 mm. Adapted from Absalao & Pimenta (2005).

1846; Ennucula puelcha d’Orbigny, 1842; and two of

Nuculanidae: Aclrana electa (A. Adams, 1846); and

Adrana patagonica (d’Orbigny, 1846).

MATERIALS AND METHODS

The material examined includes samples taken during

different cruises undertaken the South Atlantic Ocean.

The measurements used herein are commonly used in

morphometric studies with bivalves (Sibaja and Vilalo-

bos, 1986; Bonfitto and Sabelli, 1995; Gofas and Salas,

1996; Fuiman et al., 1999), and are represented in

Figure 1. The numbers of anterior and posterior teeth

were counted with the aid of a ZEISS SV-6 stereoscopic

microscope. The antero-posterior and dorso-ventral axes

of each valve were measured using a caliper of 0.05 mm

accuracy. A total of 200 valves of nuculids and 1 10 valves

of nuculanids were considered in this study (Table 1).

The statistical approach consisted of linear regression

analysis (Sokal and Rohlf, 1981). All material from this

study is deposited in the Mollusca collection of the

Departamento de Zoologia, Instituto de Biologia, Uni-

versidade Federal do Rio de Janeiro (IBUFRJ).

Table 1. Descriptive statistics of the material analyzed. Abbreviation: sd = Standard deviation.

80

A Pronucula benguelana

• Nucula semiornata

O Ennucuta puelcha

■ Adrana electa

□ Adrana patagonica

40

30

□ ft

■ □ Bj

□ q-jd-1 ^ □□□

□

rP

ID Ro D rn D

□

□

□ □

20

□P

□

□

Dorso-ventral axis (mm)

Figure 2. Relationship of dorso-ventral axis and number oi posterior teeth in studied protobranch species, lhe two families

analyzed occupy discrete morphospaces, reinforcing the importance of the number of teeth as a character at supra-specific levels.

C.D.C. Oliveira and T. H. Morales, 2010

Page 37

25

20

0)

2 15

10

5

O

0 +—

0 2 4 6 8 10 12 14

Dorso-ventral axis (mm)

Figure 3. Relationship between: A. antero-posterior and B. dorso-ventral axes with the number of anterior teeth, showing the

morphospaces overlap between Pronucula benguelana and Ennucula puelcha.

Number of posterior teeth Number of posterior teeth

Page 38

THE NAUTILUS, Vol. 124, No. 1

10

10

8

Antero-posterior axis (mm)

12

16

• (DO

0 2 4 6 8 10 12 14

Dorso-ventral axis (mm)

Figure 4. Relationship between: A. antero-posterior and B. dorso-ventral axes with the number of posterior teeth, showing the

overlap of the morphospaces of Pronucula benguelana and Nucula semiomata.

C.D.C. Oliveira and T.H. Morales, 2010

Page 39

RESULTS AND DISCUSSION

All the species studied exhibited a gradual increase of

the number of anterior and posterior teeth during on-

togeny. All results were statistically significant (Table 2),

when we compared the importance of shell size with the

number of anterior and posterior teeth. This statistical

analysis confirmed the existence of a relationship be-

tween the two variables, size and number of teeth, and

suggests that this relationship may be verified in other

protobranch species. Furthermore, it confirmed the var-

iation in the number of teeth for the same size class for

each species studied. This attests to the inconsistency of

this character when it is analyzed alone.

In addition. Figure 2 indicates a distinction among the

genera Adrana and Pronucida , Nucula, and Ennucula,

which becomes more evident when we compared the

number of posterior teeth and the length ol the dorso-

ventral axis. This result matches most accepted classifi-

cations that consider several characters (not only num-

ber of teeth) and allocate these three genera into two

distinct groups (e.g. Allen anti Hannah, 1986; Maxwell,

1988; Giribet and Wheeler, 2002; Giribet, 2008).

On the other hand, considering the Nuculidae, the

morphospace of Pronucida benguelana overlapped with

E. puelcha in the number of anterior teeth regressed

on antero-posterior axis (Figure 3a) and on dorso-

ventral axis (Fig. 3b); and P. benguelana overlapped

with N. semiomata in the number of posterior teeth

regressed on antero-posterior axis (Figure 4a) and on

dorso-ventral axis (Figure 4b). In both cases, these

overlaps of the number of teeth (anterior or posterior)

occurred up to about 4 mm in size, on each axis ana-

lyzed, for P. benguelana. Because this latter species is

about 4 mm in size, this size limit in the overlap cannot

be interpreted as a consequence of the number of

specimens collected.

It is evident that the current taxonomy of Nuculidae

presents confused generic definitions, not rare with a

great correspondence of characters. Considering only

the results presented herein, the overlaps of the mor-

phospaces of Pronucida and Nucula are in agreement,

and may reinforce the view ol Bergmans (1978), who

synonymized the two genera, or that of Allen and Han-

nah (1986), who proposed the allocation of Pronucida, at

a subgeneric rank, to the genus Nucula. Along the same

lines, the overlaps of the morphospaces of Ennucula and

Nucula may reinforce the view of Schenck (1934) who

placed Ennucula as a subgenus of Nucula. Nevertheless,

because no other taxonomic features were analyzed in

this study and, moreover, none of the species studied are

type-species of Pronucida , Nucula , or Ennucula , this

ratification of the opinions of above-mentioned authors

may lie premature.

CONCLUSION

These statistical analyses confirmed empirical observa-

tions of the relation between shell size and number of

teeth in protobranch bivalves and attests to the inconsis-

tency of the latter character when analyzed alone. For

the taxa studied herein, the number of teeth on the

hinge is an important taxonomic feature, but only when

the size of the shell is also taken into account. Other-

wise, taxonomic studies and descriptions based only on

the number of teeth without providing any measures of

the shell are not informative and might make it impossi-

ble to define whether one is dealing with several similar

species or just one that shows intraspecific variation for

the character number ol hinge teeth.

The use of other characters in the taxonomy of the

group is obviously important, but for the species studied

here, at the family level, the distinction between Adrana

(Nuculanidae) and Pronucida , Nucula , and Ennucula

(Nuculidae) is in agreement with most accepted classifi-

cations. This attests the importance of number of teeth

on the hinge related to the size ol the shell for the

distinction of these two families even when no other

characters are considered. Nevertheless, for the nueu-

lids, the differentiation ol the distinct genera is unclear.

The number of teeth on hinge and the size of the shell

alone do not provided a good distinction among the

three genera and the overlap of the morphospaces of

these different taxa reinforces the demand for the use

of more taxonomic characters and emphasizes the need

for more comprehensive studies with these groups.

ACKNOWLEDGMENTS

Our best thanks go to Dr. Ricardo Absalao (Universi-

dade Federal do Rio de Janeiro) for his encouragement

and critical information; Dr. John Zardus (Military

College of South Carolina) and Ms. Natalia Benaim

(Universidade Federal do Rio de Janeiro) for the

exchange of ideas.

O

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Reinhold Co., New York. 663 p., 24 pis.

Absalao, R.S. and A.D. Pimenta, 2005. Moluscos Marinhos da

APA do Arquipelago de Santana, Macae, RJ. Chave

Ilustrada para Identificagao das Especies do Substrato

Inconsolidado. Editora Cieneia Moderna, Rio de Janeiro.

84 p., 21 pis.

Allen, [.A. 2008. Bivalvia of the deep Atlantic. Malacologia

50(1): 57-173.

Allen, J.A. and F. J. Hannah, 1986. A reclassification of the

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Allen, |.A. and ILL. Sanders, 1973. Studies on deep-sea

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Allen, J.A. and H.L. Sanders, 1996. Studies on the deep-sea

Protobranehia (Bivalvia): the family Neilonellidae and the

family Nuculanidae. Bulletin-Natural History Museum

Zoology Series 62: 101-132.

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Bergmans, W. 1978. Taxonomic revision of Recent Australian

Nuculidae (Mollusca: Bivalvia) except Ennucula Iredale,

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Bonfitto, A. and B. Sabelli. 1995. Yoldiella seguenzae, a new

species of Nuculanidae (Bivalvia; Nuculoida) from the

Mediterranean Sea. Journal of Molluscan Studies 61:

21-27.

Coan, E.V., P.V. Scott, and F. R. Bernard. 2000. Bivalve sea-

shells of western North America: marine bivalve mollusks

from arctic Alaska to Baja California. Santa Barbara

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Cox, L. R. 1960. Thoughts on the classification of the Bivalvia.

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Dali, W. II. 1886. Report on the Mollusca. Part 1. Brachiopoda

and Peleeypoda. Reports on the results of dredging by the

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Espinosa, J. and [. Ortea. 2001. Description de una nueva

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Esteves, I.R. 1984. Recent bivalves (Palaeotaxodonta and Pter-

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Fuiman, L.A., J.D. Gage, and P.A. Lamont. 1999. Shell mor-

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nal of the Marine Biological Association United Kingdom

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Giribet, G. 2008. Bivalvia. In: Ponder, W.F. and D.R. Lindberg

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Giribet, G. and W. Wheeler. 2002. On Bivalve Phylogeny: A

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Kilburn, R.N. 1994. The protobranch genera Jupiteria,

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Maxwell, P. 1988. Comments on “A reclassification of the Re-

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THE NAUTILUS 124(l):41-43, 2010

Page 41

A new species of Zeadmete (Gastropoda: Cancellariidae)

from South Carolina, a genus previously unknown in the

Atlantic Ocean

Richard E. Petit

806 Saint Charles Road

North Myrtle Beach, SC 29582 USA

[email protected]

Lyle D. Campbell

Sarah C. Campbell

Division of Natural Sciences and Engineering

University of South Carolina Upstate

800 University Way

Spartanburg, SC 29303 USA

[email protected]

ABSTRACT

A new species of Zeadmete is described from deep water on the

Blake Plateau southeast of Charleston, South Carolina. Previ-

ously known from South Africa, New Zealand, New Caledonia,

and Fiji, this is the first report ol Zeadmete from the Atlantic

Ocean.

Additional keywords: Bathyal, deep-sea, gastropod

INTRODUCTION

The little-known genus Zeadmete has been recently

discussed by Petit and Harasewych (2000) and Bouehet

and Petit (2008). Previously known species occur off

South Africa, New Zealand, New Caledonia, and Fiji.

With the exception of Zeadmete subantarctica Powell,

1933, found at 65 m, this genus is usually found at 300-

GOO in depth. The new species extends this range to

764 meters.

Although known from only one specimen, the rarity ol

all known species, coupled with their depth, makes it

advisable to describe the species. During extensive

dredging on Norfolk Ridge (south of New Caledonia)

only one specimen of Zeadmete bilix Bouehet and Petit,

2008, was discovered although it is several times larger

than, and found in half the depth of, the new South

Carolina species.

MATERIALS AND METHODS

In 1986, Lyle and Sarah Campbell were guest scientists

with separate survey cruises on the SC Marine Re-

sources Lady Lisa to determine if Gert/on crabs were

present in sufficient quantity to support a fishery off

Charleston, South Carolina. Gert/on are found in 600

to 1200 m of water, some 160 to 320 km offshore on

the Blake Plateau. The Campbells were permitted to

add a 30 cm diameter pipe dredge to the ballast hold-

ing down the crab traps, and a series of bulk sediment

samples were obtained. Those constituted the first set

of bathyal bulk sediment samples obtained from South

Carolina waters. Mollusks were recorded by Dali

(1889, 1927) from two similar samples off Florida and

southern Georgia but there is virtually no published

documentation of this fauna from South Carolina

waters.

A sediment sample from SC Marine Resources Geryon

cruise, 23 July 1986, Blake Plateau, southeast ol Charles-

ton, South Carolina from 418 fathoms (764 meters) water

depth was recently washed for a student research proj-

ect. Bulk sediment was wet screened through seven

sieves ranging from 12.5 mm to 0.7 mm mesh. Prelimi-

nary investigation yielded 15 species of pelagic gastropods,

30 species of benthic mollusks, and other taxa ranging

from fish otoliths to diverse benthic and planktic forami-

nilera. Ongoing investigations of remaining samples will

more completely document the fauna.

One other species of Cancellariidae was found in the

same sample as the new Zeadmete, a broken specimen ol

Microcancilla microscopica (Dali, 1889).

SYSTEMATICS

Family Cancellariidae Forbes and Hanley, 1851

Genus Zeadmete Finlay, 1926

Type Species: Cancellaria trailli Hutton, 1873, by

original designation. Recent, New Zealand.

Zeadmete atlantica new species

(Figures 1-5)

Description: Shell (Figures 1-3) small (3.76 mm),

elongated biconical, consisting of 3.75 whorls. Protoconch

(Figures 4-5) smooth, evenly rounded, increasing in

Page 42

THE NAUTILUS, Vol. 124, No. 1

Figures 1-5. Z eadmete atlantica. Southeast of Charleston, South Carolina, in 418 fathoms [764 m], 1. Apertural. 2. Right lateral.

3. Dorsal views of the holotype. 4. Axial, and 5. dorsal views of protoconch. Scale bar = 1 mm for entire shell, 500 pm for protoconch

views.

diameter from 230 pm to 640 pm in 1 whorl, with fine,

irregular spiral threads evident on last 0.5 whorl. Transi-

tion to teleoconch marked by onset of axial growth striae

and fine ribs. Teleoconch of 2.75 roundly shouldered,

weakly convex whorls. Suture deeply impressed. Axial

sculpture of about 40 ribs per whorl, ribs becoming less

distinct with increasing whorl size. Spiral sculpture of

weak, narrow, evenly spaced spiral cords, about 30 on

body whorl, 15 on penultimate whorl. Aperture 0.5 shell

length, narrowly elliptical (W/L = 0.37), deflected from

coiling axis by 16 '. Outer lip strongly curved at shoulder,

evenly convex from shoulder to tip of siphonal canal.

Spiral sculpture most pronounced near shoulder and

along siphonal canal. Inner lip with smooth inductural

region that is slightly shorter than the smooth, axial

columella, which lacks columellar folds, but has a single

siphonal fold. Shell and aperture uniformly white in

color.

Type Material: Holotype USNM 1125242 (3.76x

1.96 mm).

Type Locality: Blake Plateau, southeast of Charleston,

South Carolina, 32°38.6/ N, 76°47.7' W, 764 m (Geryon

cruise, station 125, July 23, 1986).

Etymology: Named for the Atlantic Ocean.

R. E. Petit et al., 2010

Page 43

Remarks: Z eadmete atlantica new species has a more

rounded shoulder than most species in the genus.

Although corroded, the type specimen differs from its

geographically closest congener, the South African

Z. verheckeni Petit and Harasewych, 2000, in having a

rounded shoulder, more numerous axial ribs and less

prominent nodules at the intersection of axial ribs and

spiral cords. Zeadmete bathymon Bouchet and Petit,

2008, from New Caledonia has sculpture similar to

Z. atlantica but the ribs are not as numerous and the

shoulder is strongly angled.

ACKNOWLEDGMENTS

Dr. M.G. Harasewych, National Museum of Natural

History, Smithsonian Institution, Washington, DC,

kindly prepared the SEM and plate. Dr. Matthew

Campbell, Judson University, read and commented on

a draft of this paper.

LITERATURE CITED

Bouchet, P. and R.E. Petit. 2008. New species and new records

of southwest Pacific Cancellariidae (Gastropoda). The

Nautilus 122: 1-18.

Dali, W. II. 1889. [Reports on the results of dredging, under

the supervision of Alexander Agassiz, in the Gulf of

Mexico (1877-78) and in the Caribbean Sea (1879-80)

by the U.S. Coast Survey Steamer “Blake”, Lieut. -

Commander C.D. Sigsbee, U.S.N., and Commander

J.R. Bartlett, U.S.N., commanding.] XXIX. Report on

the Mollusca. Part II. Gastropoda and Scaphopoda. Bul-

letin of the Museum of Comparative Zoology, 18, 1^192,

pis. 10-40.

Dali, W.H. 1927. Small shells from dredgings off the southeast

coast of the United States by the United States Fisheries

Steamer Albatross in 1885 and 1886. U.S. National

Museum Proceedings 70 (art. 18): 1—134.

Finlay, II. [. 1926. A further commentary on New Zealand

molluscan systematics. Transactions of the New Zealand

Institute 57: 320—485, pis. 18-23.

Hutton, F.W. 1873. Catalogue of the marine Mollusca of New

Zealand, with diagnoses of the species. Colonial Museum

and Geological Survey Department, Wellington, xx + 116

pp., I pf

Petit, R.E. and M.G. Harasewych. 2000. Additions to the

cancellariid (Mollusca: Neogastropoda) fauna of South

Africa. Proceedings of the Biological Society of Washing-

ton 113: 145-154.

Powell, A.W. B. 1933. New species of marine Mollusca

from the subantarctic islands of New Zealand. Proceed-

ings of the Malacologieal Society of London 20(5),

232-236, pi. 20.

THE NAUTILUS 124(l):44-50, 2010

Page 44

Current distribution of the exotie freshwater snail Helisoma duryi

(Gastropoda: Planorbidae) in Brazil

Monica A. Fernandez

Silvana C. Thiengo

Laboratorio de Malacologia

Referenda Nacional em

Malacologia Medica

Instituto Oswaldo Cruz - Fiocruz

Av. Brasil 4365

21045-900 Rio de Janeiro, BRAZIL

[email protected]

Fernando S. M. Bezerra

Departamento de Analises Clmieas/FFOE

Universidade Federal do Ceara

Rua Capitao Francisco Pedro 1210

60430-370 Fortaleza, BRAZIL

Lucia M. S. Alencar

Secretaria de Saude do Estado do Ceara

Rua dos Tabajaras 281, Praia de Iracema

60060-510 Fortaleza, BRAZIL

ABSTRACT

This article describes the current distribution of the introduced

gastropod Helisoma duryi in Brazil. The species was recorded

for the first time in Brazil in 1972, in Formosa, state of Goias,

and since then it has been reported to occur in the states of

Ceara, Minas Gerais, Paraiba, Rio de Janeiro, and Sao Paulo.

Recently, this species was found in the state of Ceara, where it

was introduced through ornamental fish and aquatic plant

trade. The expansion of the species range in Brazil demon-

strates the need for increased efforts to monitor and con-

trol the introduction of exotic species. Up to now, H. duryi

had been found in 14 municipalities together with spec-

imens of Ampullariidae, Ancylidae, Corbieulidae, Lymnaeidae,

Planorbidae, Physidae, and Thiaridae. We believe that the

current absence of H. duryi in the localities where it had

been previously collected (1972 and 1998) could be associated

with environmental changes in those regions and also be-

cause selling in H. duryi is not as efficient as it is for other

Planorbidae species. A map with the distribution of H, duryi is

also provided.

Additional keywords: exotic freshwater mollusks, biological

invasions, invasive species, planorbids

INTRODUCTION

Non-native species, those that have been introduced

from another geographic region to an area outside its

natural range, have been the focus of several investiga-

tions in the past years, mostly because they have been

closely related to problems in human health, in the envi-

ronment, and economy. The Convention on Biological

Diversity (CBD), ratified in 188 countries, including

Brazil, is one of the most important international tools

conceived to provide environmental conventions, strate-

gies, and agreements in order to promote sustainable

development. In Brazil, where specialists and environ-

mental public bodies recognize the problems involved

with exotic species, CBD signed the Decree number

2.519, seeking to protect and manage biodiversity

(Ministerio do Meio Ambiente, 2009).

Difficulties in predicting the effects of alien species

after introduction were discussed by Meyer et al.

(2008), in an investigation on the exotic giant African

snail, Achatina fulica Bowdich, 1822. According to

Ricklefs (2005), every invasion process undergoes lour

phases: introduction or colonization; settlement, which

requires adaptation to local conditions to survive local

species interactions; geographical expansion; and even-

tual decay. The period during which every species

remains at each of those phases depends on either intrin-

sic or extrinsic factors to it. (Incidentally, Brazil is cur-

rently experiencing the explosive phase of the invasion of

A. fulica , and dense populations of that species are wide-

spread in at least 24 out of 26 Brazilian states and the

Federal District.)

In Brazil, biological invasions and the pathways of

introduction and spread of exotic species are not yet well

documented, but a number of instances of tbe spread of

invasive mollusks have been documented in the last

decade: Thiengo et al. (2007a) reported the rapid expan-

sion and current distribution of A. fulica since its intro-

duction in the state of Parana, in 1988 while Santos et al.

(2002) and Fischer and Colley (2005) reported the

occurrence of A. fulica in preservation areas in the states

of Rio de Janeiro (Ilha Grande, Angra dos Reis) and

Parana (Ilha Rasa, municipality of Guaraqueyaba), re-

spectively, and Takeda et al. (2003) and Mansur et al.

(2004) reported the occurrence of the invasive freshwa-

ter clams Limnopema fortunei (Drinker, 1857) and

Corbicula spp. in Southern Brazil. In addition to envi-

ronmental and economical problems related to exotic

snail species, some of those species have medical and

veterinary importance as they may be associated with

zoonotic and parasitic transmission ol diseases (Caldeira

et ah, 2007; Thiengo et ah, 2008).

M. A. Fernandez et al., 2010

Page 45

The aquarium trade is a major source ol exotic fresh-

water mollusks. In 1972, a population of Helisoma chinji

(Wetherby, 1879), autochthonous from the Everglades

wetlands in Florida, was first reported in Distrito de

Santa Rosa, municipality of Formosa, state of Goias,

Brazil, in natural breeding sites connected with the Cana

Brava River (Paraense, 1975). According to Paraense

(1976), these specimens collected in the locality Lagoa

da Pedra, in connection with the Cana Brava River,

included a large number of albinos obtained from sym-

patrie populations of Ampullariidae, Ancylidae, Phys-

idae, and other Planorbidae. Similarly, Thiengo et al.

(1998) also reported the presence of albino specimens

in fish tanks in the municipality of Guapimirim, state of

Rio de Janeiro, Brazil, in June 1997 and remarked the

importance of aquarium fish trade in the introduction

and spread of exotic snails in new sites.

Recognizing the threat to global biodiversity that in-

vasive species play Brazil is one of 188 countries that

have ratified the CBD in an effort to help manage this

disappearing resource. In 2006 snails were sent from

Serra Verde do Saraiva by the Secretaria de Saude of

the state of Ceara (SESA-CE), to the Centro Nacional

de Referenda em Malacologia Medica (LRNM) for

identification. These snails were identified as H. clurt/i ,

and prompted surveys of the present distribution of this

species in Brazil along with the occurrence of sympatric

freshwater snail species were performed and presented.

MATERIALS AND METHODS

Information on the distribution of Helisoma dunji in

Brazil since its first recorded introduction was obtained

from the literature and from data on specimens collected

by the authors. Field surveys were performed in three

states, from which the occurrence of H. dunji was previ-

ously reported by the staff of LRNM: Goias (munici-

palities of Formosa and Vila Boa), Rio de Janeiro

(municipality of Guapimirim), and Ceara (municipalities

of Acarape, Fortaleza, Guaiuba, and Redenyao).

In the state of Goias (Table 1), snail collections were

performed between 2003 and 2005 in wetland areas

along federal highway BR-020, and in Lagoa da Pedra,

between the municipalities of Formosa and Vila Boa. In

the state ol Rio de Janeiro (municipality of Guapimirim)

collections were made in 2000, 2003, and 2007 (Table 1)

in exotic ornamental fish ( Betta splendens (Regan. 1910))

breeding tanks. Four municipalities were investigated in

the state of Ceara (Table 1): three in the region of Serra

Verde do Saraiva (Acarape, Guaiuba and Redenyao) and

one in the Fortaleza municipality (a lake named Lagoa

de Porangabussu).

Mollusks were collected from different habitats

(streams, wells, marshy areas, fish tanks and lakes) using

collecting sieves. With the aim of assessing abiotic factors

in the habitats where IP dunji occurs, variables such

as temperature (water and air), pH, and the concen-

tration of dissolved oxygen in the water column were

measured using a mereurium thermomether, a pHmeter

(Instrutherm pH-1700), and an oxymeter (Lutron

DO-5510). Samples were maintained under laboratory

conditions at LRNM in aquaria containing dechlorinated

tap water and a thin bottom layer of a 2:1 mixture of

screened soil and ground oyster shells as a source of

mineral nutrients.

For specific identification, the snails were anesthe-

tized with 0.05% sodium pentobarbital (Hypnol®) for

five hours; killed by immersion in 70'’C water and then

fixed in Railliet- Henry solution (Fernandez et al. 2008).

Snail samples were deposited in the Malacologieal Col-

lection of Institute) Oswaldo Cruz (CM IOC).

RESULTS

In the state of Goias (Table 1), eight freshwater gastropod

species were found: Biomphalaria straminea (Drinker,

1848), Drepanotrema anatimun (Orbigny, 1835), Drepa-

notrema cimex (Morieand, 1839), Drepanotrema depres-

sissimum (Morieand, 1839), Drepanotrema hicidum

(Pfeiffer, 1839), Gnndlachia radiata (Guilding, 1828),

Melanoides tuberculatus (Muller, 1774) and Pomacea sp.

In the state of Rio de |aneiro, in the municipality of

Guapimirim (Table 1), no H. duriji specimens were

found but the following species were collected: Bio-

mphalaria tenagophiJa (d’Orbigny 1835), B. straminea ,

Hebetancylus morieand i (d’Orbigny, 1837), Lymnaea

columella Say, 1817, M. tuberculatus, Physa marmorata

Guilding, 1828, Pomacea diffusa (Reeve, 1856), and

Pomacea sp. (only juvenile specimens).

In the state of Ceara, specimens of H. dunji were

found in the two habitats, a well and a fish tank (Table 1).

In these the water temperatures were 27.3°C and

27.4°C, environment temperatures were 36.8°C and

33.7°C, pH was: 7.76 and 6.38, and dissolved oxygen

measured 7.8 mg/L and 7.0 mg/L in the well and the

fish pond, respectively. The other freshwater gastro-

pods found in the state were B. straminea, D. lucidum,

G. radiata , H. dunji , M.tuberculatus, P. marmorata ,

Pomacea lineata (Spfx in Wagner, 1827), P. diffusa, and

Pomacea sp. (only juvenile specimens).

DISCUSSION

According to Paraense (1976) and the data from

CMIOC, in August 1972, in addition to Helisoma dunji ,

the following snail species were collected in lakes form-

ed by the Cana Brava River (in the municipality of

Formosa, Goias): B. straminea, Biomphalaria schrammi

(Crosse, 1864), D. anatinum, D. lucidum, Plesioplysa

ornata (Haas, 1938), L. columella, and P. marmorata . In

the present study surveys were performed in seven

ponds formed by Cana Brava River flooded areas, in the

municipalities of Vila Boa and Formosa, but no spec-

imens of H. dunji were found.

In the 1990s, many ornamental freshwater fish breed-

ing facilities in the state of Rio de Janeiro were located in

Page 46

THE NAUTILUS, Vol. 124, No. 1

Table 1. Study localities and species found.

the municipality of Guapimirim. This probably favored

the introduction of exotic species. According to the field

work registrations in the LRNM, specimens of H. duryi

reported by Thiengo et al. (1998) were found in sym-

patry with B. straminea, Ferrissia sp., L. columella and

P. bridgesii. The latter is identified as P. diffusa nowa-

days, according to Hayes et al (2008). Many albino spec-

imens ol H. duryi and P. diffusa were also found in those

fish tanks in September, 1997. Although no PI. duryi

specimen was found, the present paper confirms the

establishment ol P. diffusa, only species reported by

Thiengo et al. (1998) and also obtained in 2007. This

species occurs naturally throughout the Amazon Basin

(Peru, Bolivia and Brazil) but it is widespread nowadays

due to aquarium and fish trade, specially the more

attractive albino specimens known as golden apple

snails.

Our results indicate a reduction in Helisoma duryi

populations in the state of Ceara. In March and May

2006, a team from Secretaria de Saude of the state of

Ceara (SESA-CE) collected samples of H. duryi in five

localities in the municipalities of Redenyao and Guaiuba,

and in the present study this species was found in only

two of these (Table 1). In the lake Porangabussu, in the

M. A. Fernandez et al., 2010

Page 47

municipality of Fortaleza, where H. duryi and M. tuber-

culatus specimens were collected in 1999 by Dr.

Fernando Bezerra (Universidade Federal do Ceara) and

sent to LRNM for identification, no specimens were

found in 2006 and 2008.

The introduction of Helisoma duriji was probably the

result of aquaculture activity. Ornamental plants are

used in fish tanks chiefly to promote water oxygenation.

These plants may transport both eggs and early stages of

freshwater gastropods, enabling their spread into new

environments. Correa et al. (1980) inferred the impor-

tance of such plants as vectors for dispersal ol non-native

mollusks, and noted that they may have been particularly

important regarding the spread of schistomsomiasis-

carrying individuals of B. straminea in Sao Paulo state.

They surveyed aquarium and aquatic plant shops through-

out the municipality and found specimens of Physidae,

Lymnaeidae, Ampullariidae, Thiaridae, and Planorbidae,

including Helisoma sp. In the same state, Franga et al.

(2007) collected sediment samples in three reservoirs of

the Baixo Rio Tiete (Promissao, Nova Avanhandava, and

Tres Irmaos), in November 2002 and August 2003, in

order to identify species of benthic mollusks. Specimens

H. duryi were found, including another exotic bivalve,

Corbicula fluminea (Mnller, 1774), and the Afro-asiatie

gastropod, M. tuberculatus. Although //. duryi was pre-

sent in the three reservoirs analyzed, that species had the

lowest density among the exotic mollusks.

For an exotic species to be regarded as invasive it must

have, at least, considerable adaptability to new environ-

ments, rapid sexual maturation, and a large reproductive

capacity (Santos et al. 2007). Ecological and parasitolog-

ical laboratory studies of Helisoma duryi obtained in

Goias in 1972 (Milward-de- Andrade, 1978a, b; Milward-

de-Andrade and Belisario, 1979; Milward-de-Andrade

and Souza, 1979; Milward-de-Andrade et al., 1979) indi-

cate adaptive advantages of that exotic species over

Biomphalaria glabrata (Say, 1818). These include a

higher reproduction rate, lower mortality, higher resis-

tance to environmental desiccation, increased starvation

survival, and increased resistance to infection by

Schistosoma mansoni in that former species.

Other authors reported that Helisoma duryi may have

the ability to control populations of Biomphalaria spp., a

vector of schistosomiasis (Frandsen, 1987; Frandsen and

Madsen, 1979), in Puerto Rico, St. Lucia, Egypt, and

Tanzania. In Brazil, Milward-de-Andrade (1979) argued

that the capacity of H. duryi to colonize Neotropical

ecosystems, either directly or indirectly, may play a

key role in the biological control of schistosomiasis

mansoni. However, throughout the last three decades,

such expected interspecific competition has not been

observed (the H. duryi population found in 1972, in

Goias, did not successfully establish itself, and was

not observed in 2003 and 2005). Remarkably, M. tuber-

culatus was found in this habitat after 2005, having been

introduced in Brazil probably by aquarists in Santos in

1967 (Vaz et ah, 1986). Currently, M. tuberculatus may

be found in seventeen Brazilian states and in the Distrito

Federal, in both lenthic and lothie habitats, with or with-

out anthropic influences (Fernandez et al., 2003).

Melanoides tuberculatus reproduces parthenogeneti-

eally, which may account for its wider geographic distri-

bution when compared to II duryi. The latter may

occasionally utilize selfing as an alternative means of

reproduction, although it is not as efficient as it is for

other Planorbidae species (Paraense and Correa, 1988).

According to these authors, H. duryi benefits much less

from functional hermaphroditism which, besides other

advantages, enables a single virgin individual to found a

new population. Furthermore, other characteristics of

M. tuberculatus , such as viviparity, iteroparity and high

survival rate of the young, may also contribute to its

spread (Santos et al., 2007).

In Guapimirim (Rio de Janeiro) and in Lagoa do

Porangabussu (Ceara), B. straminea appears to have

adapted to local conditions, forming colonies, while

H. duryi has not. Remarkably, in Guapimirim municipal-

ity, specimens of B. straminea were found in 1997 and

2003, but not in 2007; whereas B. tenagophila was

recorded in 2003 and 2007. The disappearance of

B. straminea and the establishment of B. tenagophila

must be confirmed. In contrast, Silva et al. (1997) re-

ported the replacement of B. straminea for B.tenagophila

in the municipality of Paracambi, Rio de Janeiro.

Tl le introduction of H. duryi in the state of Ceara may

be a result of B. splendens aquaculture (breeding and

trade), similar to that described for Guapimirim (Rio de

Figure 1. Helisoma duryi from Ceara state, municipality of

Redengao (04°10'46.8" S, 38°44'02.4" W).

Page 48

THE NAUTILUS, Vol. 124, No. 1

Janeiro). Ornamental and pet fish such as B. splendens

originate in Asia and were introduced to Europe and the

United States in 1874 and 1910, respectively (Faria et ah,

2006). In the 1960s and 1970s, ornamental fish breeders

in Brazil introduced production techniques and female

individuals imported from Europe and the United

States. Since then, individuals of H. clun/i have been

recorded in the following Brazilian states: Minas Gerais,

in the municipalities of Vigosa in 1967, and Uberaba

(Vidigal et ah, 2000); Rio de Janeiro, in the municipality

of Nova Iguagu in 1975; Paraiba, in the municipalities of

Joao Pessoa and Campina Grande (Abilio, 2003); and

Sao Paulo (Correa et ah, 1980; Franga et ah, 2007). The

distribution of the exotic freshwater snail H. duryi in

Brazil is shown in the Figure I .

In addition to use of the species in ornamental fish

aquaculture, Betta splendens was also released under

experimental conditions in 2000 as a biological control

of the mosquito Aedes aegypti Linnaeus, 1758, in the

state of Ceara, municipalities of Fortaleza and Caninde

(Pamplona et ah, 2004). This may in part account for the

spread of II. duryi in that state. A temporary shortage of

rainfall in the state of Ceara in October 2006 made it

difficult to find H. duryi, in contrast to March and May,

the rainfall season in that region. In October 2006, H.

duryi specimens (juvenile and eggs) were found in a fish

tank of ornamental fish production in Redengao, as well

as other snail species such as P. mannorata and P. diffusa.

Recently, Hayes et ah (2008) reported that some

ampullariid species, such as P. diffusa, may have some

characteristics that allow them to become invaders fol-

lowing introduction; its occurrence in Guapimirim (Rio

de Janeiro), ten years after its first record, supports

Hayes’s remark. Furthermore, the presence of P. diffusa

in Ceara, currently restricted to a fish tank, is reason for

concern over the potential for future spread and estab-

lishment of new colonies in other areas of Serra Verde do

Saraiva. This could happen as a result of the rainy sea-

son, a possibility that in itself makes evident the urgent

need for monitoring of the local malacofauna.

To date, there is no record of threatened native species,

risk of economical loss, or damage to public health that

could be triggered by the introduction of Heliosma

duryi in Brazil However, this lack of concern may be

unwarranted, and preventive measures against the intro-

duction and spread of the species, as well as of others that

Figure 2. Distribution of the exotic freshwater snail Helisoma duryi in Brazil: 1, Fortaleza; 2, Guaiiiba; 3, Acarape; 4, Redengao; 5,

Campina Grande; 6, Joao Pessoa; 7, Vila Boa; 8, Formosa; 9, Uberaba; 10, Vigosa; 1 1 , Promissao; 12, Sao Paulo; 13, Nova Iguagu; 14,

Guapimirim.

M. A. Fernandez et al., 2010

Page 49

are associated with environmental damages and public

health problems, should be taken. Accordingly, strict law

enforcement policies and procedures must be established

in the trade of aquatic plants to fish producers as a pre-

ventive measure to preserve our biodiversity.

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THE NAUTILUS 124(l):51-53, 2010

Page 51

Early stages of development in the endangered limpet

Patella ferruginea Gmelin, 1791 (Gastropoda: Patellidae)

Fi ee Espinosa

Georgina A. Rivera-Ingraham

Jose C. Garcia-Gomez

Laboratorio de Biologia Marina

Departamento de Fisiologia y Zoologia

Universidad de Sevilla

Avda. Reina Mercedes 6

41012 Sevilla, SPAIN

[email protected]

ABSTRACT

The larval biology of Patella fermginea is studied lor the first

time. Development in the species first showed two complete

and equal cleavages whereas the third cleavage was unequal,

resulting in an embryo with 4 micromeres and 4 macromeres.

Early troehophores were detected 19 hours post-fertilization

and pretorsional veligers appeared 27 hours post- fertilization.

Early stages of development are very similar to those shown by

other related limpet species, with higher developmental times

than those recorded for Patella caemlea and similar to those

obtained in Patella vulgata. However, in vitro fertilization and

the obtainment of spats in a massive amount could be the solu-

tion for replenishing threatened or extinct populations of this

extremely endangered Mediterranean species. The results of

the present study represent a first approach in order to produce

great amounts of spats in laboratory conditions for further

reintroduction projects aiming for conservation of the species.

Additional keywords: Conservation, endangered species

INTRODUCTION

The mollusk Patella fermginea Gmelin, 1791, endemic to

the Mediterranean, is the most endangered marine species

listed on the European Council Directive 92/43/EEC and it

is presently under serious risk of extinction ( Lahore] -

Deguen and Laborel, 1991; Ramos, 1998; Espinosa et ah,

2006). Nevertheless, its biology and ecology are poorly

known (Guerra-Gareia et ah, 2004) and studies mainly

focused on the reproductive biology and larval develop-

ment of the species are urgently required, as pointed out

by Templado (2001) and Guallart et ah, (2006), in order to

implement adequate management and conservation strate-

gies. The larval biology has not been studied in detail

before, although some preliminary fertilization assays were

made on the field by Guallart et ah, (2006). Taking into

account that in the last decades captive breeding has been

suggested an important supportive intervention to avoid the

loss of many species (IUCN, 1987), in vitro fertilization of

Patella fermginea and the obtainment of spats in a massive

amount could be the solution for replenishing the threat-

ened or extinct populations of the species around the

Mediterranean. The development of appropriate culture

techniques is considered to be crucial for die future conser-

vation of the species.

MATERIALS AND METHODS

Adults of Patella fermginea were collected from Ceuta,

North Africa (35°53/20" N, 5°18'30" W), during October

and November 2006, overlapping with the annual repro-

duction period of the species (Frenkiel, 1975) and inde-

pendently of the lunar cycle, but always during low tide.

Animals were kept in an aquarium, at a constant tempera-

ture of 18°C. Additionally, and in order to determine the

maturation stage of the gonads, biopsies were taken. The

gonads of ripe animals were dissected for artificial insemi-

nation following Van den Biggelaar (1977) and Wanninger

et ah (1999) protocols; all further fertilization, culture, and

breeding procedures were carried out in Seachem B artifi-

cial seawater filtered through a 0.45 pm mesh (AFSW) at

18°C. 1000 ml beakers were used as culture vessels, each

filled with 500 ml of AFSW, stirred through moderate

aeration. Eggs from four females were treated with alka-

line sea water (pH = 8.9, by addition of drops of NH4OH)

for 1-7 minutes before fertilization to induce the egg-

ripening process, followed by stirring, allowed to settle for

3 minutes, washing, and decanting 4 or 5 times (see also

Dodd, 1957). Sperm of four males was diluted in AFSW

until the suspension became fully clear; the agility of sperm

cells was confirmed under the microscope before insemi-

nation. For fertilization, 10-20 drops of sperm suspension

were used per liter of egg-containing AFSW. The percent-

age of fertilized eggs at each treatment was assessed

using a compound microscope by the presence of normal

or abnormal cleavage in 100 undamaged eggs that were

Page 52

THE NAUTILUS, Vol. 124, No. 1

5

Figures 1-5. Development stages in Patella ferruginea , reared at 18°C. Light micrographs. 1. First cleavage (2 h) displaying polar

body (pb). 2. Eight-cell stage (4 h). Micromeres (mic); macromeres (mac). 3. >12 cells: morula (5 h). 4. Completely formed

trochophore (19 h) with apical cilia (ae), prototrochal cilia (pc), prototrochal girdle (pg) and stomodeum (sto). 5. Early pretorsional

veliger (27 h) with apical cilia (ac), prototrochal girdle (pg) and larval shell (Is). Scale bars 100 pm.

randomly sampled from each vessel at least 4 h after

insemination (see Baker and Tyler, 2001).

Larval cultures were kept in AFSW with 50 mg strep-

tomycin and 60 mg penicillin per litre to minimize

microbial or fungal infection. The water was changed

periodically by pouring the vessels’ content on to a sieve

of 100 pm being held partly under water to prevent

damage to the larvae. Larval development was moni-

tored with a compound microscope, and major stages

were recorded with photomicrographs.

RESULTS

Eggs of Patella ferruginea present an average diameter

of 149.78 pm whereas sperm shows an average length of

3.78 pm (Espinosa et ah, 2006). The first evidence of

fertilization was the extrusion of the first polar body in

the first two hours after insemination, and the complete-

ness of the first two cleavages, equal and always initiated

near the polar body (Figure 1). However, the fertilization

rate resulted very low (3±1%). The third cleavage was

F. Espinosa et al., 2010

Page 53

unequal and equatorial, such that the resulting 8-celled

embryos were composed ol 4 macromeres and 4 micro-

meres (Figure 2). Trocophores presented the natural

morphology associated with the taxon and swam actively

during 19 hours after fertilization, with telotroeh (anal

tuft), apical and prototrochal cilia (Figure 4) well devel-

oped and similar to those described for other patellid

limpet species. In early trochophores, steady swimming

was often alternated with abrupt bursts of speed. This

sprint behaviour was constantly observed. Trochophores

swam horizontally and vertically in culture vessels.

The stomodeum was visible immediately beneath the

prototrochal girdle (Figure 4). In pretorsional veliger

the larval shell started to be observed (Figure 5) 27 hours

after fertilization, whereas other structures remained, as

the apical cilia and prototrochal girdle. This pretorsional

veliger could be observed until 48 hours after fertiliza-

tion, when the remained larvae died.

DISCUSSION

The early stages of larval development in Patella

ferruginea obtained in the present study, appear to

be veiy similar to other related limpet species, with

higher developmental times than Patella caerulea (see

Wanninger et al., 1999) and similar to those obtained in

Patella vulgata (see Dodd, 1957; Wanninger et al., 1999).

Nevertheless, it is known that water temperature influ-

ences the timing of developmental events (Kay and

Emlet, 2002). In this sense, the proportional timing for

P. ferruginea could be higher than for P. vulgata, al-

though further experiments would be necessary. It is

important to note that the fertilization rates obtained

were very low and that the larval survival did not exceed

48 h, despite the use of similar methods that have

reported good results in other related species (Dodd,

1957; Wanninger et al., 1999, 2000; Kay and Emlet,

2002). Further studies are required in order to establish

if these results can be imputed to the necessity of

improving the methodology or to biological constraints

of the species.

Either way, the results of the present study could be

considered as a first step towards the elaboration of a

protocol that will permit to rear spats in laboratory con-

ditions which could be used for further reintroduction

and eonservational projects.

ACKNOWLEDGMENTS

This work was funded by a postdoctoral grant of the

Ministry of Education of Spain awarded to F. Espinosa

(EX2006-0534), predoctoral grant of the Ministry of

Education of Spain to G.A. Rivera-Ingraham (AP-2006-

04220) and financial support by the “Autoridad Portuar-

ia de Ceuta”. The authors express their gratitude to

“Consejerfa de Medio Ambiente-Obimasa,” Ceuta, for

its support.

LITERATURE CITED

Baker, M.C. and P.A. Tyler. 2001. Fertilization success in

the commercial gastropod Haliotis tuberculata. Marine

Ecology Progress Series 21 1 : 205-213.

Dodd, J.M. 1957. Artificial fertilisation, larval development

and metamorphosis in Patella vulgate L. and Patella

caerulea L. Pubblicazione di la Stazione Zoologica di

Napoli 29: 172-186.

Espinosa, F., J.M. Guerra- Garcia, D. Fa, and J.C. Garcia-

Gomez. 2006. Aspects of reproduction and their implica-

tions for the conservation of the endangered limpet.

Patella ferruginea. Invertebrate, Reproduction and Devel-

opment 49: 85-92.

Frenkiel, L. 1975. Contribution a l’etude des cycles de repro-

duction des Patellidae en Algerie. Pubblicazione di la

Stazione Zoologica di Napoli 39: 153-189.

Guallart, J., J. Templado, M. Calvo, P. Cabezas, I. Acevedo,

A. Machordom, and A. A. Luque. 2006. Inventario

y seguimiento de Patella ferruginea en Espana, asi

conro la elaboration de una propuesta de estrategia de

conservation de la especie. Informe final. Ministerio de

Medio Ambiente, Madrid, 199 pp.

Guerra-Garcia, J.M., |. Corzo J., F. Espinosa, and J.C. Garcia-

Gomez. 2004. Assessing habitat use of the endan-

gered marine mollusc Patella ferruginea (Gastropoda,

Patellidae) in nordiern Africa: preliminary results and

implications for conservation. Biological Conservation

116: 319-326.

IUCN (International Union for Conservation of Nature and

Natural Resources). 1987. The IUCN position statement

on traslocation of living organisms: introductions, re-intro-

ductions and re-stocking. IUCN Council, Gland, Switzer-

land, 4 September 1987, 20 pp.

Kay, M.C. and R.B. Emlet. 2002. Laboratory spawning, larval

development, and metamorphosis of the limpets Lottia

digitalis and Lottia asmi (Patellogastropoda, Lottiidae).

Invertebrate Biology 121: 11-24.

Laborel-Deguen, F. and ]. Laborel. 1991. Statut de Patella

ferruginea Grnelin en Mediterranee. In: Boudouresque,

C.F., M. Avon and V. Gravez (Eds.). Les Especes marines

a proteger en Mediterranee. GIS Posidonie Publishers,

Marseille, pp. 91-103.

Ramos, M.A. 1998. Implementing the Habitats Directive for

mollusc species in Spain. Journal of Conchology Special

Publication 2: 125-132.

Templado, J. 2001. Patella ferruginea (Grnelin, 1791). In:

Ramos, M.A., D. Bragado and J. Fernandez (Eds.). Los

invertebrados no insectos de la Directiva Habitats en

Espana. Ediciones Serie Tecniea, Organismo Autonomo

Parques Nacionales, Direction General de Conservation

de la Naturaleza, Ministerio de Medio Ambiente, Madrid,

pp. 41—49.

Van Den Biggelaar, J. A. M. 1977. Development of dorsoventral

polarity and mesentoblast determination in Patella

vulgata. Journal of Morphology 154: 157-186.

Wanninger, A., B. Ruthensteiner, S. Lobenwein, W. Salvenmoser,

W. Dictus, and G. Haszprunar. 1999. Development of

the musculature in the limpet Patella (Mollusca, Patello-

gastropoda). Development, Genes and Evolution 209:

226-238.

Wanninger, A., B. Ruthensteiner, and G. Haszprunar. 2000.

Torsion in Patella caerulea (Mollusca, Patellogastropoda):

ontogenetic process, timing, and mechanisms. Inverte-

brate Biology 1 19: 177-187.

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THE0NAUTILUS

CONTENTS

Volume 124, Number 2

July 7, 2010

ISSN 0028-1344

Paul Valentich-Scott

Carol Skoglund

Jess VV. Jones

Richard J. Neves

Axel Alf

Philippe Maestrati

Philippe Bouchet

B.L. Bodamer

M.L. Ostrofsky

Claude Vilvens

Javier Sellanes

Roland Houart

Robert Moffitt

A review of the Recent Pandoridae (Bivalvia) in the Panamic Province, with

descriptions of three new species 55

Descriptions of a new species and a new subspecies of freshwater mussels,

Epioblasma ahlstedti and Epioblasma florentina aureola (Bivalvia: Unionidae),

in the Tennessee River drainage, USA 77

New species of Bolma (Gastropoda: Vetigastropoda: Turbinidae) from

the tropical deep sea 93

The use of aquatic plants by populations of the zebra mussel ( Dreissena

polymorpha ) (Bivalvia: Dreissenidae) in a small glacial lake 100

Description of Calliostorna ceciliae new species (Gastropoda: Chilodontidae:

Calliotropinae) from off Chile 107

Anew Scabrotrophon (Gastropoda: Muricidae) from Hawaii and discussion

about the generic classification ol Boreotrophon kamchatkanus Dali, 1902,

a related species 112

THE NAUTILUS 124(2):55-76, 2010

Page 55

A review of the Recent Pandoridae (Bivalvia) in the Panamic

Province, with descriptions of three new species

Paul Valentich-Scott

Carol Skoglund

Santa Barbara Museum of Natural History

2559 Puesta del Sol Road

Santa Barbara, CA 93105 USA

[email protected]

[email protected]

ABSTRACT

Six genera and 16 species of Panamic Pandoridae are described

and illustrated. Three species are described as new, namely

Pandora ( Pandora ) rachaelae , Pandora ( Pandorella ) sarahae,

and Clidiophora dorsorectus , and one new genus, Coania.

Diagnoses are provided for the genera, subgenera, and species,

as well as illustrations of the type specimens of the nominate

species. Frenanuja , Clidiophora , Heteroclidus, and Foveadens

are herein elevated to generic rank. The high diversity of

Pandoridae in the tropical Panamic Province is compared with

other tropical regions along with more temperate climes.

INTRODUCTION

The Greek myth of Pandora portrays her as the first

mortal woman, one of exceptional beauty. Pandora also

opened the forbidden box, releasing all the evils of

humankind. So it is with the members ol the biv; live

family Pandoridae, species of amazing beauty, but also

those with taxonomic confusion and peril. We herein

review the Pandoridae of the Panamic Province, accom-

panied by full descriptions, diagnostic characters between

genera and species, and provide photographs of types and

typical specimens.

The functional morphology of the Atlantic Pandora

inaequivalvis (Linnaeus, 1758) and P. pinna (Montagu,

1803) was detailed by Allen (1954). The biology and

functional morphology of the Pacific P. filosa was exam-

ined by Thomas (1994). Through experimental studies,

Allen and Allen (1955) postulated that the primary life

position of P. inaequivalvis is with the curved side down,

but the species is capable of surviving in almost any

orientation for considerable periods. However, Allen

and Allen also noted that specimens buried more than

2 cm below the sediment surface had a low rate ol sur-

vival, which likely limits the distribution ol most Pandora

to low energy habitats. Additional pandorid functional

morphology was elucidated by Yonge and Morton

(1980) and Morton (1984), with particular emphasis on

the ligament and lithodesma. The functional morphology

and natural history of all Panamic Pandoridae remains

undocumented.

In their monograph ol the Western Atlantic Pandoridae,

Boss and Merrill (1965) presented the first modem review

of the family in the New World. Due to a paucity ol

literature at the time, they postulated that the family is

not diverse in the tropical regions, a hypothesis which will

be refuted by the data herein. Importantly, Boss and Mer-

rill provided detailed anatomical descriptions and precise

illustrations to accompany their shell moiphology descrip-

tions. Unfortunately, subsequent workers did not follow

the dentition and ligament nomenclature defined in this

important paper.

Boss (1965) included all known generic, subgeneric,

specific, and subspecific names in the Pandoridae. This

has provided a base for our current research, in particu-

lar with documenting generic and subgeneric names.

Panamic pandorids were first described by G.B.

Sowerby, I (1835), in his review of new species collected

by Cuming in South America. Carpenter (1856, 1865)

described additional species from Mexico, and Dali

(1915) added more species from Mexico and Panama.

Keen (1958) presented the first complete accounting ol

the Panamic pandorids, including diagnoses ol Pandora

subgenera and illustrations ol several type specimens, and

slightly revised this treatment thirteen years later (Keen,

1971). Olsson (1961) provided keys to the southern

Panamic Pandora subgenera and species, and extended

the geographic distribution of several species.

Thus, with the seemingly ardent work by the authors

above, we were perplexed to have great difficulty iden-

tifying common pandorid species in the Panamic Prov-

ince. When examining museum and private collections

we found that the identifications were almost random,

with little continuity between identifications, sometimes

even within a single collection. Upon examination ol the

type specimens ol the Panamic species, we further

noted that most of the species in collections were incor-

rectly identified. It was with this backdrop that we

Page 56

THE NAUTILUS, Vol. 124, No. 2

developed the diagnoses below, with a goal of providing

useful tools to identify this difficult and plastic group of

bivalves.

Abbreviations and Text Conventions: Each valid

taxon is followed by a synonymy, a description, distribu-

tion and habitat data, information on tvpe specimens and

type locality, and additional remarks about the taxon.

Distribution information is based on Recent specimens

we have examined, unless otherwise noted. We have not

examined any fossil material. Sadly, no wet preserved

specimens were located during this study, thus we did

not describe the anatomy of the species covered below.

All references to valve convexity and concavity refer to

the external Hew the specimens.

Abbreviations used in the text are as follows: BMNH -

The Natural Histoiy Museum, London, United King-

dom; CAS - California Academy of Sciences, San

Francisco, California, USA; LACM - Natural History

Museum of Los Angeles County, Los Angeles, Califor-

nia, USA; MCZ - Museum of Comparative Zoology,

Harvard University, Cambridge, Massachusetts, USA;

PRI - Paleontological Research Institution, Ithaca, New

York, USA: SBMNH - Santa Barbara Museum of Natu-

ral Histoiy, Santa Barbara, California, USA; UMiVIL -

University of Miami Marine Laboratory, Rosenstiel

School of Marine and Atmospheric Science, Miami,

Florida, USA; USNM - National Museum of Natural

History, Smithsonian Institution, Washington DC, USA.

SYSTEM ATICS

Pandoridae Rafinesque, 1815

Diagnostic characters between genera and subgenera

are given in Table 1, and species-level characters are

given in Table 2.

Genus Pandora Bruguiere, 1797

Pandora Bruguiere, 1797. Type species (SD Children,

1823): Pandora rostrata Lamarck, 1818, = Salem

inaequivalvis Linnaeus, 1758. Recent, Mediterranean.

Description: Shell strongly inequilateral, posterior

end longer; right valve flat to concave; left valve flat to

convex; hinge plate vestigial to well developed, with

weak to strong cardinal teeth bordering resilifer;

lithodesma usually present; sculpture of irregular

commarginal striae or ribs, some with radial ribs or

grooves; interior nacreous. Siphons short.

Distribution: The genus is cosmopolitan in distribu-

tion, found from intertidal to abyssal depths.

Remarks: Considered by Boss and Merrill (1965) to

be primarily a cold-water genus, the findings in this

paper indicate a high tropical diversity. It is likely other

tropical regions have a much higher diversity than cur-

rently reported.

Subgenus Pandora sensu stricto

Hinge of left valve narrow, gready reduced, anterior car-

dinal tooth a small tubercle or broadly flattened, posterior

cardinal tooth absent to reduced. Right valve with small to

moderate anterior cardinal tooth, posterior tooth short to

moderately long. Exterior sculpture of commarginal striae

or ribs, some wit 1 1 very faint radial striae.

Pandora ( Pandora ) brevifrons G.B. Sowerby I, 1835

(Figure 1)

Pandora brevifrons G.B. Sowerby I, 1835: 93.

Description: Shell Shape: Ellipsoid-elongate; very

inequivalve, left valve veiy inflated, right valve very con-

cave; entire shell strongly twisted dorsoventrally; anterior

end short; anterodorsal margin straight; posterior end

attenuate, without discrete rostrum; ventral margin of left

valve broadly rounded, slightly straighter mid-ventrally.

Sculpture and Color: Anterior end of left valve not set

off by a change in sculpture or color; left valve with 2 low

radial ribs extending from beaks to posterior margin,

commarginal striae over entire valve; right valve sculp-

ture of fine commarginal striae, with long, deep, furrow

along posterodorsal margin.

Hinge: Left valve with anterior tubercle, and an elon-

gate, oblique resilifer; right valve with two short, sub-

equal cardinal teeth; lithodesma unknown.

Muscle Scars: adductor muscle scars subequal,

subcircular.

Length: to 22 mm [BMNH].

Distribution: Currently only known from the type

locality at Bahia Panama, Panama (9.0°N) [BMNH].

Type Material: BMNII 1966572, 3 syn types - paired

valves.

Type Locality: Panama, 18 m (originally 10 fathoms),

sandy bottom.

Remarks: Records from the region around San Felipe,

Baja California, Mexico (Gemmell et ah, 1987; Dushane

and Brennan, 1969) are Pandora sarahae new species.

In spite of intensive collecting in Panama, this species

has not been found since its description in 1835. It is

possible that the type is mislocalized. However, study of

specimens from adjacent and far reaching provinces has

also not yielded any material of this species.

Literature: Keen (1971: 287), Olsson (1961: 454).

Pandora (Pandora) rachaelae new species

(Figures 2-4)

Description: Shell Shape: Ovate-elongate; inequivalve,

left valve slightly inflated, right valve flat; posterodorsal

margin of light valve overlapping left, ventral margin of left

valve overlapping right; entire shell not twisted to slightly

twisted; anterior end short; anterodorsal margin slightly

recurved; posterior end broadly rounded, with wide, short,

truncate rostrum; ventral margin broadly rounded, with

P. Valentich- Scott and C. Skoglund, 2010

Page 57

Table 1. Generic and subgeneric characteristics of the Pandoridae in the Panamic Province.

Genus

(Subgenus)

Sculpture of

valves

Left hinge

Pandora

( Pandora )

right valve

commarginal only

Right hinge

Pandora right valve with

( Pandorella ) radial grooves

anterior tooth, ends anterior of

adductor scar

Clidiophora

right valve

commarginal only

anterior tooth, ends anterior of

adductor scar

Foveadens

right valve

commarginal only

right valve with

radial grooves;

left valve with

radial ribs

Coania

(Continued)

Taxa

Shell Shape

Left Valve Dentition

Right Valve Dentition

Clidiophora

cornuta

Frenamya

radians

Clidiophora

claviculata

Clidiophora

dorsorectus

Foveadens

panamensis

Coania rhypis

Heteroclidus

punctata

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THE NAUTILUS, Vol. 124, No. 2

Figures 1-4. 1. Pandora brevifrons, syntype, BMNH 1966572, Panama, sandy bottom, 18 m; length = 22 mm. 2-4. Pandora

rachaelae new species, 2. Holotype, SBMNH 347835, Mexico, Baja California Sur, off Cabo Pulmo, 23°26'00" N, 109°25/21" W, 13-

17 m; length = 13.9 mm. 3—4. Paratypes, SBMNH 84939, same locality as holotype; 3. Length = 14.5 mm, 4. Length = 14.2 mm.

shallow indentation approximately one-third of total length

from anterior end.

Sculpture and Color: Left valve sculpture of

commarginal striae and irregular, low commarginal

undulations; left valve with one low radial rib extending

from beaks to posterior margin, in some top of rib

with granules or nodes; in most, anterior end of left

valve demarcated by change in color, without sulcus;

right valve sculpture of commarginal striae, with wide

commarginal undulations in some, long furrow along

posterodorsal margin weak to absent.

Hinge: Left valve with anterior tubercle, and a short

obique resilifer; right valve with two cardinal teeth; anterior

tooth short, curved in some, not reaching posterior end of

anterior adductor muscle scar; posterior toodi, thin, elon-

gate, paralleling dorsal margin; lithodesma thin, narrow.

Muscle Scars: Both adductor muscle scars subcircular.

Length: To 14 mm [SBMNII].

Distribution: Los Frailes, Baja California Sur

(23.4°N) [SBMNH], to San Felipe, Baja California

(31.0° N) [SBMNH], to Puerto Huatulco, Oaxaca

(15.8° N) [CAS], Mexico; also at Isla Socorro, Islas Revil-

lagigedo, Colima, Mexico (18.8° N) [CAS]; intertidal

zone to 60 m, sand [SBMNH].

Type Material: Holotype SBMNH 347835, length =

13.88 mm, height = 6.18 mm, coll, by Carl and Laura Shy,

January 1969. Paratypes: SBMNH 84939, same locality as

P. Valentich- Scott and C. Skoglund, 2010

Page 61

holotype, 3 pairs; USNM 1132899, same locality as holo-

type, 1 pair. Additional paratypes: CAS 181543, 6 pairs,

Mexico, Colima, Islas Revillagigedo, Isla Socorro, 20 m.

Type Locality: Mexico, Baja California Sur, off Cabo

Pulmo, 23°26'00" N, 109°25'21" W, 14-18 m (originally

7-9 fathoms).

Etymology: Named in honor of the senior author’s

oldest daughter, Rachael Gwinn, in thanks for her con-

tinual support and positive attitude.

Comparisons: This species has a more compressed

left valve than P. brevifrons, has a more ventrally sloping

anterodorsal margin, and has a broader, more tubercular

anterior cardinal tooth.

Literature and Additional Records: Not seen in

previous literature. This species has frequently been

misidentified in museum and private collections as

Pandora brevifrons or P. gramdata. SBMNH has 13

additional lots.

Pandora ( Pandora ) uncifera Pilsbry and Lowe, 1932

(Figure 5)

Pandora uncifera Pilsbry and Lowe, 1932: 104.

Description: Shell Shape: Ellipsoid-elongate; equi-

valve, both valves compressed, flat; anterior end short;

anterodorsal margin curved ventrally in a distinctive

hook; posterior end attenuate, with wide, moderately

long, truncate rostrum; ventral margin broadly rounded

to straight, except for broad, shallow indentation approx-

imately one-third of length from anterior end.

Sculpture and Color: Anterior end of left valve demar-

cated by change in color, without sulcus, commarginal

striae and undulations over entire surface, more sub-

dued anteriorly; left valve with one very low, broad

radial rib extending from beaks to posteroventral mar-

gin; right valve sculpture of wide commarginal undula-

tions, broad region on posterodorsal margin with vertical

striations.

Hinge: Left valve with two cardinal teeth, anterior tooth

moderately short, posterior tooth elongate, paralleling

dorsal margin; right valve with two weak cardinal teeth,

anterior tooth narrow, moderately short, posterior tooth

elongate, narrow, resilifer narrow, oblique; lithodesma

moderately thick, narrow.

Muscle Scars: Both adductor muscle scars subcircular

to subovate.

Length: To 13 mm [SBVINII],

Distribution: Bahia de las Palmas, Baja California Sur

(23.7°N), north to Bahia San Luis Gonzaga, Baja Califor-

nia (29.8°N) [SDNHM, CAS], and Cabo Tepoca, Sonora

(30.3°N) [SBMNH], Mexico, to Manta, Manabi, Ecua-

dor (0.9°S) [PRI]; 5-66 m [SBMNH],

Type Material: Holotype ANSP 155632.

Type Locality: Acapulco, Guerrero, Mexico, 37 m

(originally 20 fathoms).

Literature: Gemmell et al. (1987: 61-62), Hertlein

and Strong (1946: 97), Keen (1971: 287), Olsson (1961:

454), Pilsbry and Lowe (1932: 104-105).

Subgenus Pandorella Conrad, 1863

Pandorella Conrad, 1863. Type species (M): Pandora

arenosa Conrad, 1834. Miocene, Virginia.

Kennerlia Carpenter, 1864. Type species (SD Stoliczka,

1870): Pandora(Kennerlia) bicarinata Carpenter, 1864,

= P. bilirata Conrad, 1855. Recent, California. Kennerleijia ,

Kennerlijia, Kenerlyia, Kenerleyia, of authors, unintentional

alterations of an established name.

Description: Hinge of left valve greatly reduced, ante-

rior cardinal tooth a small tubercle or broadly flattened,

posterior cardinal tooth absent to reduced. Right valve

with two cardinal teeth; anterior small to moderate; pos-

terior short to moderately long. Lithodesma present.

External sculpture of right valve with radial grooves

or ribs.

Remarks: Tl ae dentition ol this subgenus is very

similar to that of Pandora s.s. The prime distinguishing

character of Pandorella is the presence of radial ribs or

grooves in the right valve.

Other eastern Pacific Ocean species in this subgenus

include Pandora (Pandorella) bilirata Conrad, 1855,

P. (P) filosa (Carpenter, 1864), P. ( P. ) glacialis Leach,

1819, and P. ( P. ) wardiana A. Adams, 1860.

Pandora (Pandorella) gramdata Dali, 1915

(Figure 6)

Pandora gramdata Dali. 1915: 449.

Description: Shell Shape: Subquadrate to subovate;

inequivalve, left valve moderately inflated, right valve

flat to concave; anterodorsal margin straight; anterior

end produced, sharply rounded; posterior end only

slightly attenuate, some with very broad, short, sub-

truncate rostrum; posterodorsal margin straight; right

valve overlapping left along posterodorsal margin; ven-

tral margin broadly rounded, with shallow indentation.

Sculpture and Color: Anterior end ol left valve

demarcated by change in sculpture, without sulcus,

with a few commarginal undulations on anterior end,

central and posterior slopes with commarginal striae

only; left valve with two sharp, narrow, radial ribs

extending from beaks to posterior margin, with strong

commarginal ribs overlying radials forming nodes,

granules or scales on some; right valve sculpture of

veiy fine commarginal striae, with few to many

(1-10) fine radial grooves that are less prominent or

numerous in juveniles.

Hinge: Left valve with one short, obscure anterior cardi-

nal tooth; right valve with two cardinal teeth; anterior

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THE NAUTILUS, Vol. 124, No. 2

Figures 5-6. 5. Pandora uncifera, SBMNH 347838, Mexico, Baja California Sur, off Cabo Pulmo, 23°26'00" N, 109°25'21" W,

1.3-17 m; length = 13 mm. 6. Pandora granulata , syntype, USNM 211348, Mexico, Baja California Sur, off La Paz, 24° 18' N, 110°22' W,

48 m; length = 7.2 mm.

short, stout; posterior thin, elongate, paralleling dorsal

margin; some right valves with additional internal rib,

near end of posterior cardinal, paralleling dorsal margin;

ligament narrow, short, oblique; lithodesma broad, stout,

short.

Muscle Scars: Anterior adductor muscle scar ovate-

elongate, posterior scar subcircular.

Length: To 10 mm [SBMNH],

Distribution: La Paz, Baja California Sur (24.2° N)

[USNM], into the Golfo de California as far north as

Puerto Libertad, Sonora (29.9°N) [SBMNH], to

Teacapan, Sinaloa (22.2°N) [SBMNH], Mexico; 15-80

m [LACM, SBMNH], in sand and mud [SBMNII].

Type Material: USNM 211348, syntypes, about 100

open valves, about 12 closed pairs.

Type Locality: Off La Paz, Baja California Sur, Mex-

ico, 24° 18' N, 1 10° 22' W, 48 m (originally 26.5 fathoms),

broken shell bottom (Albatross 2823).

Remarks: Synonymized in error by Valentich-Scott

(1998) and Coan et al (2000). Pandora bilirata Conrad,

1855, has more prominent radial grooves on the exterior

of the right valve and does not have granulations on the

radial ribs of the left valve.

Literature: Keen (1971 : 289).

Pandora ( Pandorella ) radiata G.B. Sowerby, 1835

(Figure 7)

Pandora radiata G.B. Sowerby I, 1835: 94; P. (. Kennerlia )

bicarinata Carpenter, 1864: 638; 1865: 603; P. (. Kennerlyia )

convexa Dali, 1915: 449.

Description: Shell Shape: Subovate; left valve mod-

erately to highly inflated, right valve flat to very concave,

deeply fitting inside left valve; anterodorsal margin with

nearly straight slope, slightly upturned on end; posterior

end broadly subtruncate, with short broad rostrum in

some specimens; posterodorsal margin straight; right

valve moderately overlapping left along posterodorsal

P. Valentich-Scott and C. Skoglund, 2010

Page 63

margin; ventral margin broadly rounded, with shallow to

significant indentation towards anterior end.

Sculpture and Color: Anterior end of left valve demar-

cated by shallow sulcus, entire surface of irregular

commarginal striae, some with low, broad, obscure radial

ribs; left valve with one narrow radial rib extending from

beaks to posterior margin, frequently eroded in larger

specimens, some specimens with faint dorsal rib; right

valve sculpture of very fine commarginal striae, and

strong, widely spaced radial grooves.

Hinge: Left valve with one long, obscure anterior cardi-

nal tooth, in some hinge plate depressed anterior of

tooth; right valve with two cardinal teeth; anterior tooth

short, stout; posterior tooth thin, elongate, wider ven-

trally; ligament narrow, moderately short, oblique;

lithodesma broad, thick.

Muscle Scars: Both adductor muscle scars subequal,

subcircular.

Length: To 31 mm [USNM],

Distribution: Catalina Island, Los Angeles County,

California (33.5°N) [USNM], into the Golfo de Cali-

fornia as far north as Isla Smith, Baja California

(29.1°N) [SBMNH] and Cabo Lobos, Sonora (29.9°N)

[SBMNH], Mexico, to Zorritos, Tumbes, Peru (3.5°S)

[SBMNH]; 20-170 m [SBMNH],

Type Material: Pandora radiata : BMNH 1964469,

holotype, one pair; Pandora bicarinata : USNM 592440,

1 pair mounted on glass slide; Catalina Island, California.

Pandora convexa : USNM 171068, syn types, 2 pairs; oil

lower California, Ballenas, Mexico [Puerto Abreojos,

Baja California Sur], 10 m (originally 5.5 fathoms),

Albatross 2835, 26°42'30"N, 113°34,15"W.

Type Locality: Insularum Muerte, Columbiae

Occidentalis [Isla del Muerto, Guayas, Ecuador],

Remarks: The relationship with Pandora bilirata

Conrad, 1855, should be examined more thoroughly,

preferably with molecular data. It is possible that this

northern species is a junior synonym of P. radians.

Literature: Hertlein and Strong (1946b: 97-98, as

P. convexa ), Keen (1971: 289-291).

Pandora ( Pandorella ) sarahae new species

(Figure 8)

Pandora brevifrons G.B. Sowerby I, of authors , not

G.B. Sowerby I, 1835

Description: Shell Shape: Ellipsoid-elongate; veiy

inequivalve, left valve veiy inflated, right valve veiy

concave; entire shell slightly to moderately twisted

dorsoventrally; anterior end short; anterodorsal margin

slightly recurved in most; posterior end attenuate, with

short, subtruncate rostrum; ventral margin ol left valve

straight to slightly rounded, broadly curved along

anteroventral and posteroventral margins.

Sculpture and Color: Anterior end of left valve set off by

a change in sculpture, with commarginal striae anterior of

beaks, and fine commarginal ribs posterior of beaks,

extending over posterior end, with fine sulcus demarcat-

ing the two regions; left valve with one moderate radial

rib extending from beaks to posterior margin, with heavy

commarginal ribs extending across it to the dorsal margin;

right valve sculpture of fine commarginal striae, with long,

deep, wide furrow along posterodorsal margin, larger spec-

imens with irregular radial grooves near ventral margin.

Hinge: Left valve with two teeth; anterior tooth low,

thickened tubercle; posterior tooth short, thin, extending

anterior of ligament; ligament long, oblique, with thin

groove or thickening posterior to it; lithodesma veiy thin,

narrow; right valve with two cardinal teeth; anterior

tooth stout, short, curved, not reaching posterior portion

of anterior adductor muscle scar; posterior tooth long,

thin, paralleling dorsal margin.

Muscle Scars: Anterior adductor muscle scar sub-

trigonal to subcircular, posterior subcircular.

Length: To 12 mm [SBMNH],

Distribution: Bahia Magdalena, Baja California Sur

(24.6°N) [SBMNH] and San Felipe, Baja California

(31.0°N) [SDNHM], Mexico; 2-10 m, sand [SDNHM,

SBMNH],

Type Material: Holotype SBMNH 84940, length =

12.04 mm, height = 5.09 mm. collected by Carol and

Paul Skoglund, October 1979. Paratypes, locality same

as holotype: SBMNPI 84941, 3 specimens; SBMNH,

2 specimens; CAS 181988, 1 specimen, length = 10.63

mm; USNM 1132897, 1 specimen, length = 11.13 mm;

Paratypes, SDNHM 90076, Mexico, Baja California, San

Felipe, 10 specimens.

Type Locality: Mexico, Baja California Sur, Balria

Magdalena, Puerto San Carlos, 24°48'7.60" N,

1 12°7' 17.61" W, 2-10 m, in sand.

Etymology: Named in honor of the senior author’s

youngest daughter, Sarah Gwinn, who has a keen biolog-

ical spirit, and a twisted sense of humor.

Comparisons: No other Panamie pandorid has the

strong lateral twisting found in P. sarahae. In comparison

to P. granulata , P. sarahae has a narrower, more produced,

anterior end, and fewer radial grooves on the exterior of

the right valve. Pandora radiata is much wider dorsoven-

trally than either of the two aforementioned species, and

lias more, deeper radial grooves in the right valve. Pan-

dora rachaelae is not twisted, and most specimens are

compressed.

Literature: Gemmell et al. (1987: 6 1 , as P. brevifrons).

Genus Frenamya Iredale, 1930

Frenamya Iredale, 1930. Type species (OD): Coelodon

patulus Tate, 1889. Recent, Australia.

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THE NAUTILUS, Vol. 124, No. 2

Figures 7-8. 7. Pandora radiata , holotype, BMNH 1964469, Ecuador, Guayas, Isla del Muerto; length 13 mm. 8. Pandora

sarahae , holotype SBMNH 84940, Mexico, Baja California Sur, Bahia Magdalena, Puerto San Carlos, 24°48,7.60"N, 112° 7/17.61,/

W, 2-10 m, sand; length = 12 mm.

Coelodon Carpenter, 1865, non Audinet-Serville, 1832.

Type species (SD Stoliczka, 1871): Pandora ceylanica

G.B. Sowerby I, 1835. Recent, Ceylon.

Description: Shell strongly inequilateral, posterior

end longer; right valve flat to concave; left valve flat to

convex. Hinge of left valve with strong, moderate to long

anterior cardinal tooth. Right valve with 3 cardinal teeth,

the central cardinal strong, elongate to diamond shaped.

Lithodesma absent. External sculpture of eommarginal

striae or ribs only.

Frenamya arcuata (G.B. Sowerby I, 1835)

(Figures 9-15)

Pandora arcuata G.B. Sowerby I, 1835: 93.

Description: Shell Shape: Ham-shaped; left valve

moderately inflated, right valve flat to slightly concave,

not fitting inside left valve; anterior end relatively short;

anterodorsal margin with straight, strong trigonal serra-

tions in most large specimens; posterior end strongly

rostrate; posterodorsal margin moderately to very

strongly recurved, some more recurved posteriorly; right

valve overlapping left along posterodorsal margin, more

so near posterior end; ventral margin evenly rounded,

almost circular, without indentation.

Sculpture and Color: Anterior end of left valve demar-

cated by veiy slight change in color, with shallow sulcus

in some, eommarginal striae over entire surface, with

one or two veiy low eommarginal undulations in some;

P. Valentieh- Scott and C. Skoglund, 2010

Page 65

Figures 9-15. 9-14. Frenamya arcuata, syntypes, BMNH 1964467, Ecuador, Guayas, Santa Elena; 9, 13 length = 22 mm;

10 length = 27 mm; 11, 12 length — 25 mm. 15. Frenamya arcuata , SBMNH 119375, Mexico, Baja California Sur, Bahia Santa

Maria, 24°44'0" N, 112° 12' W, 15 fm; length 14 mm.

left valve with one low, broad radial rib extending from

beaks to posterior margin, with strong commarginal bars

crossing posteriorly; right valve sculpture of veiy fine

commarginal striae, with shallow posterodorsal groove,

and rib dorsal to it; right valve without change in color on

anterior end.

Hinge: Left valve with three cardinal teeth; anterior

tooth long, curved ventrally directed, widest near beaks,

ending at the top ot the anterior adductor scar; central

tooth very small, short, directly below beaks; posterior

tooth very thin, moderately long, paralleling dorsal

margin; without furrow posterior to ligament; ligament

moderately long, broad, oblique; right valve with three

cardinal teeth; anterior thin, long, curved, extending to

top of anterior end of muscle scar; central tooth moder-

ately short, very stout, diamond shaped, slightly bifid;

posterior thick, slightly granulate on top, moderately

elongate, paralleling dorsal margin, reaching only half

way to posterior adductor muscle scar.

Muscle Scars: Anterior adductor muscle scar

subcircular, posterior scar ovate-elongate, posterior scar

almost touching dorsal margin.

Length: To 26 mm [SBMNH], reported in literature to

40 mm [Keen, 1971], but no specimens ol this length

were found.

Distribution: In the Gulf of California as far north as

Bahia Santa Maria, Baja California Sur, Mexico (24.7° N)

[SBMNH], south to Maneora, Tumbes, Peru (4.1° S)

[UMML, CAS]; 15-30 m [SBMNH],

Type Material: BMNH 1964467/1-3, syntypes, 3 left

valves.

Type Locality: Ecuador, Guayas, Santa Elena.

Remarks: Unfortunately the type specimens of

F. arcuata are only left valves, which has led to

many misinterpretations of the species. We have found

it to be much less common than previously reported.

Page 66

THE NAUTILUS, Vol. 124, No. 2

Olsson (1961: Plate 81, figs, la-g) figured a number

of species as a single species, and Keen (1971) followed

this lead.

The record of F. arcuata in Keen (1971) from

Laguna Ojo de Liebre, on the Pacific side of Baja

California Sur, remains unverified. Specimens of this

species were not located from that locality at CAS,

which would be the likely repository for specimens that

Keen vouchered.

Literature: Carpenter (1865: 596-597), Hertlein and

Strong (1946: 98, as P. cristata), Hertz et al. (1985), Keen

(1971: 287), Olsson (1961: 456).

Frenamija cristata (Carpenter, 1865)

(Figure 16)

Clidiophora cristata Carpenter, 1865: 597

Description: Shell Shape: Subovate-elongate; both

valves compressed, twisted to right posteriorly; left

valve moderately convex, right valve slightly concave;

anterodorsal margin straight, sloping ventrally, some

with veiy weak serrations; posterior end attenuate, with

short, truncate, well-demarcated rostrum especially in

right valve; posterodorsal margin strongly arcuate; right

valve overlapping left along posterodorsal margin; ven-

tral margin broadly rounded, without indentation.

Sculpture and Color: Anterior third of left valve demar-

cated by change in color, without sulcus, commarginal

striae over anterior end; left valve with one heavy broad

to narrow radial rib extending from beaks to posterior

margin, with shallow groove ventral to it; right valve

sculpture ol very fine commarginal striae, and irregular

low commarginal undulations.

Hinge: Left valve with two cardinal teeth; anterior

elongate, narrow, anteroventrally directed towards

anterior end of anterior adductor muscle scar; posterior

tooth very thin, moderately short, adjacent to the dorsal

margin; right valve with three cardinal teeth; anterior

elongate, narrow; central tooth short, stout; posterior

tooth, elongate, narrow thin, not granulate on top,

paralleling dorsal margin; ligament moderately wide,

oblique, short; without furrow between ligament and

posterior tooth.

Muscle Scars: Adductor muscle scars subequal, anterior

subcircular, posterior ovate-elongate.

Length: To 24 mm [BMNH],

Distribution: Only known from the type locality in

the Golfo de California, Mexico (general type locality)

[BMNH], Records from Guatemala and El Sal-

vador reported by Hertlein and Strong (1946: 98)

remain unverified. Likely these were confused with

P. arcuata.

Type Material: Holotype BMNH 1963441, 1 pair.

Type Locality: Gull of California, Mexico.

Frenamija radians (Dali, 1915)

(Figures 17-19)

Pandora ( Coelodon ) radians Dali, 1915: 450; P. arcuata

G.B. Sowerby I, auctt. non G.B. Sowerby I, 1835.

Description: Shell Shape: Subovate-elongate; left

valve slightly to moderately inflated, l ight valve flat to

slightly concave, fitting inside left valve; anterior end

moderate to long; anterodorsal margin with straight to

broadly rounded, with strong trigonal serrations in large

specimens; posterior end attenuate, with narrow, moder-

ately long, truncate rostrum; posterodorsal margin

evenly recurved; right valve overlapping left along

posterodorsal margin; ventral margin broadly rounded,

without indentation.

Sculpture and Color: Anterior end of left valve demar-

cated by change in color, without strong sulcus,

commarginal striae over entire surface, some with a few

commarginal undulations; left valve with one veiy low,

veiy broad radial rib extending from beaks to posterior

margin; right valve sculpture of veiy fine commarginal

striae, with deep posterodorsal groove.

Hinge: Left valve with one long, thin to stout, ventrally

directed anterior cardinal tooth, widest near beaks, end-

ing at top of anterior adductor scar; long, narrow furrow

posterior to ligament; ligament narrow, oblique; right

valve with three cardinal teeth; anterior long, thin; cen-

tral tooth short, stout, diamond shaped; posterior thin to

thick, smooth to granulate on top, veiy elongate,

paralleling dorsal margin, not quite reaching posterior

adductor muscle scar.

Muscle Scars: Both adductor muscle scars nearly

circular, posterior scar moderately close to dorsal

margin .

Length: To 24 mm [SBMNH],

Distribution: Puerto Abreojos, Baja California Sur

(26.8° N) [USNM], and Bahia Jolotemba, Nayarit, Mex-

ico (21.4° N) [CAS, Kaiser Collection], to Zorritos,

Tumbes, Peru (3.5° S) [Olsson, 1961]; 4-300 m

[SBMNH, CAS], mud [SBMNH],

Type Specimens: USNM 171053, holotype, 1 open

pair; off lower California, Ballenas, Mexico [Puerto

Abreojos, Baja California Sur], 10 m (originally 5.5

fathoms), Albatross 2835, 26°42'30" N, 113034'15" W.

Literature: Dali (1915: 450-451), Keen (1971: 289),

Olsson (1961: plate 81, figure Id as P. arcuata).

Genus Clidiophora Carpenter, 1864

Clidiophora Carpenter, 1864. Type species (OD): Pan-

dora claviculata Carpenter, 1856. Recent, tropical east-

ern Pacific.

Description: Shell strongly inequilateral, posterior

end longer; right valve flat to concave; lelt valve flat

to convex. Hinge of left valve with veiy strong, long

P. Valentich-Scott and C. Skoglund, 2010

Page 67

Figures 16-19. 16. Frenamya cristata , holotype, BMNH 1963441, Mexico, Gulf of California [general locality]; length = 22.5 mm.

17. Frenamya radians , holotype, USNM 171053, Mexico, Baja California Sur, Puerto Abreojos, 26°42,30// N, llS^l'lS" W, 10 m;

lengtli = 15.5 mm. 18-19. Frenamya radians , SBMNH 360635, Mexico, Jalisco, Bahia Tenacatita, Caleta de Los Angeles, 6—20 m;

Figure 18, length = 20 mm; Figure 19, length = 24 mm.

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THE NAUTILUS, Vol. 124, No. 2

Figures 20-21. 20. Clidiophora claviculata , syntype, BMNH 1962052, Mexico, Sinaloa Mazatlan; length = 44.5 mm.

21. Clidiophora claviculata, SBMNH 347854, Mexico, Sonora, off Bahia Kino, 28°47,06" N, 111°57'16" W, 13 m; length = 45 mm.

anterior cardinal tooth, which ends posterior of the

anterior adductor muscle, posterior tooth veiy long,

thin. Right valve with two or three cardinal teeth, the

central cardinal very small or absent. Lithodesma

present. External sculpture of commarginal striae or

ribs only

Clidiophora claviculata (Carpenter, 1856)

(Figures 20-21)

Pandora claviculata Carpenter, 1856: 228.

Description: Shell Shape: Variable from subovate-elon-

gate to subquadrate; both valves compressed, left valve

slightly concave or convex, right valve flat to slightly

convex or concave; most specimens twisted to the

left; anterodorsal margin straight to curved, rarely with

very weak serrations; posterior end broadly rounded to

straight, with short, truncate, upturned, well-demarcated

rostrum; posterodorsal margin straight to strongly re-

curved; right valve slightly overlapping left along pos-

terodorsal margin; ventral margin broadly rounded,

without indentation.

Sculpture and Color: Anterior half to two thirds of

left valve demarcated by change in color in some, with-

out sulcus, commarginal striae over posterior end,

becoming more prominent anteriorly, worn specimens

with weak radials posteriorly; sculpture of both valves

of irregular commarginal undulations and striae; both

valves with one heavy broad radial rib extending from

beaks to posterior margin, with deep groove ventral

to it.

Hinge: Left valve with three teeth; anterior tooth

elongate, broad, ventrally directed, ending posterior of

P. Valentich-Scott and C. Skoglund, 2010

Page 69

anterior adductor muscle scar; central tooth short to

moderate in length, thin; posterior tooth very elongate,

narrow, some granulate on top, directed to dorsal portion

of posterior adductor muscle scar; ligament narrow,

oblique, long; lithodesma broad, long; long, narrow fur-

row between ligament and posterior cardinal tooth; right

valve with two cardinal teeth; anterior tooth moderate to

long, narrow dorsally, wide medially, narrow ventrally,

sometimes with secondary tooth projecting past middle

of anterior adductor muscle scar; posterior tooth thin,

very elongate, paralleling dorsal margin, most granulate

or serrate on top.

Muscle Scars: Both adductor muscle scars subcircular,

posterior scar larger, region dorsal to anterior scar thick-

ened in many.

Length: To 45 mm [BMNH],

Distribution: Laguna Manuela, outer coast of Baja

California Sur (28.2° N) [CAS], into the Golfo de Califor-

nia to near its head at San Felipe, Baja California

(31.0°N) [SDNJIM, SBMNH, CAS] and Puerto

Pehasco, Sonora (31.3°N) [SBMNH], south to Mazatlan,

Sinaloa (23.2°N) [BMNH], Mexico; 15-60 m [SBMNH],

Type Material: BMNH 1962052/1-3, syntypes, 3 pairs.

Type Locality: Mazatlan, Sinaloa, Mexico.

Remarks: Olsson (1961: 456) and Keen (1971: 287)

synonymized Clidiophora claviculata with Frenamya

arcuata. Clidiophora daviadata is much more com-

pressed and has the anterior tooth in the left valve

directed to the posterior portion of the anterior adductor

muscle scar when compared to F. arcuata. When com-

pared to C. comuta, C. clavicidata has a more arcuate

posterodorsal margin and a longer rostrum.

Clidiophora claviculata is perhaps the most variable in

shell outline of all of the Panamic pandorid species. The

type series is very quadrate in overall shape, but com-

monly specimens we have examined are more ovate-

elongate, with a longer rostrum. With further study, it is

possible that more than one species might be present

in this group. Based on the curvature of the shell and

rostrum, this species appears to lay with its right side

on the sediment, unlike most other Panamic pandorid

species, which lay on their left side.

Literature: Gemmell et al. ( 1987: 62-63, as P. comuta ),

Hertz et al. (1985).

Clidiophora comuta (C. B. Adams, 1852)

(Figures 22-23)

Pandora comuta C. B. Adams, 1852: 519 [repr.: 295], ex

Gould ms; Clidiophora acutedentata Carpenter, 1865:

598, nomen vanum (an unjustified intentional emenda-

tion of an established name).

Description: Shell Shape: Subovate; both valves

compressed, twisted to left posteriorly; left and right

valves slightly convex, right valve slightly concave in

some; anterodorsal margin straight and sloping ventrally

to slightly curved; posterior end straight to broadly

rounded, rostrum short or absent; posterodorsal margin

straight, some slightly arcuate terminally; right valve

narrowly overlapping left along posterodorsal margin;

ventral margin broadly rounded, without indentation.

Sculpture and Color: Anterior half to two-thirds of left

valve diagonally demarcated by change in color, without

sulcus; left valve sculpture of irregular commarginal

striae, with one heavy broad radial rib extending

from beaks to posterior margin, without shallow groove

ventral to it; right valve sculpture of irregular

commarginal striae, with moderately broad groove

paralleling dorsal margin; escutcheon absent to long,

narrow, shallow.

Hinge: Left valve with three cardinal teeth; anterior

tooth elongate, broad, ventrally directed, ending in mid-

dle of posterior side of anterior adductor muscle; central

tooth very small, short, not well demarcated in small

specimens; posterior tooth thin, very elongate, removed

from dorsal margin; right valve with two cardinal teeth;

anterior tooth short, broad; posterior tooth, elongate,

narrow, not granulate on top, removed from dorsal mar-

gin; ligament moderately wide, oblique, very long;

lithodesma broad, long; with slight furrow between liga-

ment and posterior tooth.

Muscle Scars: Adductor muscle scars subequal,

subcircular.

Length: To 36 mm [SBMNH],

Distribution: Laguna Ojo de Liebre, Pacific Coast oi

Baja California Sur (27.8°N) [SBMNH], into the Golfo

de California as far north as San Felipe, Baja California

(31.0°N) [SBMNH], and offshore south of Bahia la

Choya, Sonora (31.0°N) [CAS], Mexico, to Panama

[MCZ]; intertidal zone to 70 m [SBMNH],

Type Material: MCZ 186309, holotype (broken),

1 pair.

Type Locality: Panama (no specific locality).

Remarks: This species is the most common species

found in the museum collections, and perhaps is the

most common large species in the Panamic Province.

It has been mislabeled in collections as Pandora

claviculata, P. panamensis , and P. radians.

Carpenter (1865) renamed this species on the grounds

that C. B. Adams’ name was misleading, having been

based on a broken type specimen that appeared to be

“cornuate”, e.g. to have posterior horns.

Literature: Hertz et al. (1985), Keen (1971: 289),

Olsson (1961: 455).

Clidiophora dorsorectus new species

(Figure 24)

Description: Shell Shape: Subovate-elongate, very

fragile, thin, translucent; both valves compressed, left

Page 70

THE NAUTILUS, Vol. 124, No. 2

Figures 22-23. 22. Clidiophora comuta, liolotype, MCZ186309, Panama [no specific locality]; length, 16 mm. 23. Clidiophora

cornuta , SBMNH 83351, Mexico, Sonora, off Bahia Kino, 28°47' N, 111°58' W, 55 m; length = 37 mm.

valve flat to slightly convex, right valve flat to slightly

concave; most specimens flat, few twisted slightly to the

left; anterodorsal margin straight, not curving ventrally,

slightly recurved dorsally, without serrations; posterior

end broadly to narrowly rounded, rostrum poorly

defined, when visible, short, broad; posterodorsal margin

straight; right valve slightly overlapping left along

posterodorsal margin; ventral margin broadly rounded,

expanded posteriorly, without indentation.

Sculpture and Color: Left valve not demarcated by

change in color, without sulcus; sculpture of left valve

of coinmarginal striae and irregular commarginal undula-

tions, stronger posteriorly; left valve with one sharp,

broad radial rib extending from beaks to posterior margin,

fine commarginal ribs from radial rib to dorsal margin.

Hinge: Lett valve with three cardinal teeth; anterior

tooth moderately long, moderately broad, ending about

one-third of length of the posterior side ol the anterior

adductor muscle scar; medial tooth short, moderately

narrow; posterior tooth thin, very elongate, angling well

down from dorsal margin, granulate on top, not quite

reaching dorsal end of posterior adductor muscle scar;

dorsal to posterior tooth a deep furrow extending from

beaks to posterior margin; right valve with two cardinal

teeth; anterior tooth short, slightly curved, ventrally

directed, ending well short of posterior end of anterior

P. Valentich-Scott and C. Skoglund, 2010

Page 71

Figures 24-25. 24. Clidiophora dorsorectus , holotype, SBMNIl 83944, Mexico, Baja California Sur, off Punta la Gringa;

29.0321° N, 113.5196° W; 20-40 fathoms [40-80 m]; length = 34 mm. 25. Heteroclidns punctata, SBMNIl 118713. California, San

Diego County, Coronado Island, intertidal; length = 47 mm.

adductor muscle scar; posterior tooth very elongate,

narrow, granulate on top, directed to dorsal portion ol

posterior adductor muscle scar; ligament long, narrow,

oblique; lithodesma broad, thick.

Muscle scars; Anterior adductor muscle scar

subcircular, posterior scar ovate-elongate, region dorsal

to anterior scar not thickened.

Length: To 34 mm [SBMMH],

Distribution: In the Golfo de California at Punta la

Gringa, Baja California (31.3°N) [SBMNH], and Isla

Danzante, (24.7°N) [SBMNH], Baja California Sur,

Mexico; 20-90 m [SBMNH],

Type Material: Holotype SBMNH 84944, length =

33.96 mm. Height - 19.79 mm, collected by Carol and

Paul Skoglund from 1976 through 1993, from type local-

ity. Paratypes, from type locality, SBMNH 84945 (1 spec-

imen); CAS 181987, 1 specimen, length = 21.61 mm;

USNM 1132898, 1 specimen, length = 21.12 mm.

Paratypes, Mexico, Baja California Sur, west of Isla

Danzante, 25. 794660° N, 1 1 1.281876°W; 30-45 m; col-

lected by Carol and Paul Skoglund, 1984; SBMNH 4

specimens.

Type Locality: Mexico, Baja California, off Punta la

Gringa; 29.0321° N, 1 13.5196° W; 40-80 m (originally

20-40 fathoms).

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THE NAUTILUS, Vol. 124, No. 2

Etymology: Named alter the diagnostic feature - a

straight dorsal margin - dorsorectus.

Remarks: Like Pandora clavicidata, this species

appears to lay with its right side on the sediment, unlike

most other Panamic Pandora species, which lay on their

left side.

Literature: Not seen in previous literature.

Genus Heteroclidus Dali, 1903

Heteroclidus Dali, 1903. Type species (OD): Pandora

punctata Conrad, 1837. Recent, California.

Description: Hinge of left valve with veiy strong,

long anterior cardinal tooth, which ends anterior of the

anterior adductor muscle, posterior tooth very long, thin,

paralleling dorsal margin. Right valve with three cardinal

teeth, the central cardinal robust, long. Lithodesma

present. External sculpture ol commarginal striae or

ribs only.

Heteroclidus punctata (Conrad, 1837)

(Figure 25)

Pandora punctata Conrad, 1837: 228.

P[andora], (Heteroclidus) p. g abbi Dali, 1903: 1521.

Description: Shell Shape: Subovate-oblique; both

valves compressed, both valves slightly convex, left slightly

more convex than right; anterodorsal margin broadly

rounded, without serrations; posterior end broadly

rounded, with short, truncate, poorly defined rostrum;

posterodorsal margin strongly arcuate; right valve

overlapping left along posterodorsal margin; ventral margin

broadly rounded, with indentation towards anterior slope.

Sculpture and Color: Anterior third of left valve demar-

cated by change in color and sculpture, with very shallow

sulcus, anterior end with irregular commarginal striae and

fine granules; posterior two-thirds with commarginal striae;

left valve with one veiy low, broad radial rib extending

from beaks to posterior margin, with shallow groove ven-

tral to it; right valve sculpture of veiy fine commarginal

striae, and irregular commarginal undulations.

Hinge: Left valve with two cardinal teeth; anterior tooth

elongate, thick, anteroventrally directed; posterior tooth

short, narrow, obscure; ligament long, moderately wide,

oblique; lithodesma broad, thick, long; right valve with

three cardinal teeth; anterior tooth long, narrow; central

tooth long, broad; posterior tooth, elongate, narrow.

Muscle Scars: Adductor muscle scars subequal,

subcircular; both valves with irregular, widely spaced

punctuations dorsal to pallial line.

Length: To 47 mm [SBMNH],

Distribution: Esperanza Inlet, Vancouver Island,

British Columbia (49.9°N) [RBCM], to Punta Pequena,

Pacific coast of Baja California Sur, Mexico (26.2°N)

[LACM]; subtidal zone to 50 m [SBMNH], in mud.

Known from the middle Pliocene ol California.

Type Material: BMNH 1966304, possible holotype,

1 left valve.

Type Locality: Santa Barbara, California, USA.

Literature: Carpenter (1865: 598), Coan et al. (2000:

520), Grant and Gale (1931: 262-263), Hertlein and

Grant (1972: 336), Keen (1971: 289).

Genus Foveadens Dali, 1915

Foveadens Dali, 1915. Type species (OD): Pandora

( Foveadens ) panamensis Dali, 1915. Recent, tropical

eastern Pacific.

Description: Hinge of left valve with two short,

curved anterior cardinal teeth; posterior tooth long, par-

tially united with the dorsal margin with a septum. Right

valve with three cardinal teeth; anterior cardinal small,

tubercular; central short, bulbous; posterior elongate.

Lithodesma absent. External sculpture of commarginal

striae or ribs only.

Foveadens panamensis (Dali, 1915)

(Figures 26-27)

Pandora ( Foveadens ) panamensis Dali, 1915: 451.

Description: Shell shape: Subquadrate to subovate;

both valves very compressed, both valves slightly convex,

right slightly more convex than left; anterodorsal margin

straight, without serrations; posterior end subtruncate,

with short, truncate, poorly defined rostrum; postero-

dorsal margin straight near beaks, slightly upturned pos-

teriorly; right valve overlapping left along posterodorsal

margin; ventral margin broadly rounded, with indenta-

tion towards anterior slope.

Sculpture and Color: Anterior third of left valve demar-

cated by change in color and sculpture in fresh spec-

imens, anterior end opaque, posterior end translucent,

with veiy shallow sulcus, anterior end with irregular

commarginal ribs and striae; posterior two-thirds with

weak radial and commarginal striae; left valve with one

heavy broad radial rib extending from beaks to posterior

margin, with shallow groove ventral to it; right valve

sculpture of very fine commarginal striae, and irregular

commarginal undulations.

Hinge: Left valve with three cardinal teeth; anterior tooth

short, stout, trigonal, ventrally directed; central tooth, veiy

short, narrow; posterior tooth elongate, fused to dorsal

margin near beaks, forming tunnel between tooth and

dorsal margin; ligament moderately wide, oblique, short;

without furrow between ligament and posterior tooth;

right valve with two cardinal teeth; anterior tooth short,

stout, directed towards middle ol anterior adductor mus-

cle; posterior tooth, elongate, veiy thick, sinuous in some;

right valve with an additional minute anterior cardinal

visible in some specimens.

Muscle Scars: Both adductor muscle scars subovate,

posterior slightly larger.

P. Valentich-Scott and C. Skoglund, 2010

Page 73

Figures 26-27. 26. Foveadens panamensis, holotype, USNM 252276, Panama, “Old Panama,' intertidal; length — 19 mm.

27. Foveadens panamensis , SBMNH 83338, Panama, “Old Panama,” intertidal; length 23 mm.

Length: To 26 mm [SBMNH],

Distribution: This species is uncommon in collec-

tions, known from Ciudad Panama, Panama (9.0°N)

[SBMNH, USNM, UMML], and Archipelago de las

Perlas, Panama (approximately 8. 5°N) [Olsson, 1961].

Type Material: USNM 252276, holotype, 1 opened

pair, badly damaged;

Type Locality: Old Panama, Panama, beach drift.

Literature: Hertlein and Strong (1946: 98), Keen

(1971: 289), Olsson (1961: 457).

Coania new genus

Type Species: Pandora ( Kennerlia ) rhypis Pilsbry and

Lowe, 1932: 105.

Description: Hinge of left valve with three cardinal

teeth; two moderately short, straight anterior teeth; poste-

rior tooth of moderate length, some slightly united with

the dorsal margin with a septum. Right valve with two

cardinal teeth; anterior cardinal modertately short, stout;

posterior tooth elongate, stout. Lithodesma present. Ante-

rior end of left valve strongly demarcated with notch.

External sculpture of left valve with radial sculpture cen-

trally and posteriorly; right valve sculpture of fine

commarginal striae and weak, irregular radial grooves.

Etymology: Named in honor of Eugene V. Coan, for

his tremendous contributions to our understanding of

the eastern Pacific Ocean Bivalvia.

Distribution: Thus far only known from the type

locality of the type species, in El Salvador.

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THE NAUTILUS, Vol. 124, No. 2

Figure 28. Coania rhypis , paratype, SBMNH 39009, El Salvador, La Union, Golfo de Fonseca, La Union; length 24 mm.

Comparisons: The distinct radial sculpture on the left

valve and arrangement of the cardinal teeth separate

Coania from all other genera in the family.

Coania rhypis (Pilsbry and Lowe, 1932)

(Ligure 28)

Pandora ( Kennerlia ) rhypis Pilsbry and Lowe, 1932: 105.

Description: Shell Shape: Subovate-oblique;

inequivalve, left valve slightly larger, moderately inflated,

right valve flat; anterior end relatively long; anterodorsal

margin gently bowed; posterior end veiy broadly

rounded, with short, narrow, truncate rostrum;

posterodorsal margin slightly recurved; ventral margin

broadly rounded, with deep, broad indentation towards

anterior end.

Sculpture and Color: Anterior end of left valve strongly

demarcated with notch, anterior end with irregular

commarginal striae, central slope with narrow, moder-

ately spaced radial ribs, becoming obscure posteriorly in

some specimens; left valve with two narrow to broad

radial ribs extending from beaks to posterior margin;

right valve sculpture of veiy fine commarginal striae,

and a few weak, irregular radial grooves, most evident

ventrally.

Hinge: Left valve with three cardinal teeth, two teeth

anterior of ligament, one longer posterior tooth; ligament

narrow, oblique; lithodesma narrow, thin; right valve

with two cardinal teeth, moderately elongate, anterior

tooth slightly bifid.

Muscle Scars: Anterior adductor muscle scar

subcircular, posterior ellipitical.

Length: To 25 mm [SBMNH],

Distribution: Only known from the type locality at

La Union, Golfo de Fonseca, El Salvador (13.4°N)

[SBMNH, ANSP]; 80 m [ANSP].

Type Material: ANSP 155503, holotype, 1 open pair.

T\pe Locality: La Union, Gulf of Fonseca, El

Salvador.

Literature: Keen (1971: 291), Pilsbry and Lowe

(1932: 105).

DISCUSSION

Surprisingly little attention has been paid to understand-

ing the taxonomy of members of the Pandoridae, within

the Panamic Province, as well as globally. They are not

an uncommon component of the offshore bivalve fauna.

Perhaps it is their fragile, laterally flattened shell that has

led to the lack of interest. Or possibly, as we have

encountered, dealing with the variability of shells shapes

leads one to give up in disgust. Whatever the reason, we

hope that this work will encourage other bivalve taxono-

mists to tackle the group in their geographic region.

With 16 pandorid species found in the Panamic Prov-

ince, one can postulate that there is likely much

unexplored diversity in other tropical and temperate

regions around (he world. Mikkelsen and Bieler (2007)

P. Valentich-Scott and C. Skoglund, 2010

Page 75

only reported three species of Pandora from southern

Florida, even with extensive offshore collecting. Simi-

larly, Lamprell and Healey (1998), found only two

pandorids in all of Australia. Oliver (1992) included two

species living in the Red Sea, and further stated that the

“Pandoridae is a small group of bivalves. . .' The Chinese

coastline includes only three species ol pandorids

(Valentich-Scott, 2003; Xu, 2004), and only four species

are reported from Japanese waters (Okutani, 2000).

We have found the best diagnostic identification char-

acters to be in the hinge, rather than the overall shell

shape or inflation. We also suspect if live specimens or

wet presewed material becomes available, additional

anatomical characters will immediately become appar-

ent. Molecular data will undoubtedly yield further

advancement in the understanding of this challenging

group of bivalves.

ACKNOWLEDGMENTS

We are very thankful to Ellen Strong (National Museum

of Natural History, Smithsonian Institution), Paul

Callomon (Academy of Natural Sciences, Philadelphia),

and Kathie Way (The Natural History Museum,

London) for allowing access to their general and type

collections, and providing excellent workspace to

examine and photograph specimens. We wish to grate-

fully thank the following individuals and institutions for

the loan of specimens; Adam Baldinger (MCZ), Carole

and Jules Hertz, Elizabeth Kooks (CAS), Nancy Voss

(UMML), Lindsey Groves (LACM), and Margi Dyke ns

(SDNHM). Eugene Coan provided useful comments on

an early draft oi this manuscript. Andre Sartori critically

reviewed the manuscript, and provided many helpful

observations and suggested modifications. Patricia Sa-

deghian took digital photographs ol all non-type spec-

imens, and assisted with image editing and preparation.

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THE NAUTILUS 124(2):77-92, 2010

Page 77

Descriptions of a new species and a new subspecies of freshwater

mussels, Epioblasma ahlstedti and Epioblasma florentina aureola

(Bivalvia: Unionidae), in the Tennessee River drainage, USA

Jess W. Jones

U.S. Fish and Wildlife Service

Department of Fisheries and Wildlife Sciences

Virginia Polytechnic Institute and State University

Blacksburg, VA 24061 USA

[email protected]

Richard J. Neves

Department of Fisheries and Wildlife Sciences

Virginia Polytechnic Institute and State University

Blacksburg, VA 24061 USA

ABSTRACT

A new species and a new subspecies of Epioblasma are de-

scribed from the Tennessee River drainage, USA. Epioblasma

ahlstedti (Duck River Dartersnapper) currently is restricted

to the Duck River in west-central Tennessee (TN). However,

museum collections indicate that the species likely occurred in

the Buffalo River, TN, a tributary to the Duck River, and in the

Tennessee River at Muscle Shoals, Alabama (AL), and lower

Shoal Creek, AL. The following diagnostic morphological char-

acteristics of E. ahlstedti are based on the female: (1) pro-

nounced posterior-ventral shell expansion of the adult female

shell; (2) slate-gray to dark-purple mantle-pad; (3) spongy tex-

ture of the mantle-pad; and (4) display of a single, tan-colored

micro-lure that moves slowly side-to-side. Epioblasma florentina

aureola (Golden Riffleshell) currently is restricted to Indian

Creek, a tributary to the upper Clinch River, Virginia. Histori-

cally, the species occurred in numerous tributaries in the Ten-

nessee River drainage downstream at least to the Duck River.

The following diagnostic morphological characteristics of

E. florentina aureola are based on the female: (1) gray mantle-

pad with a black mottled background; and (2) mantle-pad is

pustuled but the pustules are rounded. The genus Epioblasma

represents the most endangered group of freshwater mussels in

North America; 18 of the recognized 25 species or subspecies

are already extinct. Likewise, these newly described species and

subspecies are critically endangered and despite being listed as

endangered under the Endangered Species Act remain in need

of focused conservation to prevent their extinction.

Additional keywords: Endangered, molecular DNA markers,

phylogenetic analysis, Tennessee River basin

INTRODUCTION

The Tennessee River and its tributaries support the most

species-rich mussel assemblage in North America (NA)

(Figure 1), with 102 species known historically from the

system (Parmalee and Bogan, 1998). Unfortunately, pol-

lution and hydrological modifications (e.g., dams) to the

river system over the past 100 years have reduced mussel

diversity to approximately 80 extant species (Parmalee

and Bogan, 1998; Williams et al., 2008). The decline of

species belonging to the genus Epioblasma was the most

severe (Johnson, 1978). Of the 18 species and subspecies

known from the system, only four remain, and of those

lost, most are considered extinct and one is extirpated

but remains in a small isolated population in Ohio. Spe-

cies in this genus have specialized reproductive traits,

including species with shell morphologies and mantle-

lures that can attract and capture their fish hosts to

facilitate infestation by the gloehidia (Jones et al., 2006;

Barnhart et al., 2008). Epioblasma shells are character-

ized by small to medium sizes (~30-70 mm) and sexual

dimorphism. The posterior- ventral end of the female

shell is expanded, to form a distinct protrusion, or an

area of the shell herein termed, the shell expansion

(Figures 2, 3, 5, 8). This distinctive feature of female

Epioblasma was considered by Walker (1910) to be the

“highest expression of unionid development. The shell

expansion houses a modified portion of the mantle,

known as the mantle lure that functions to attract host

fish. The focal species of the current study belong to the

Epioblasma subgenus Tondosa (Johnson, 1978), which

have a prominent shell expansion and a mantle-lure that

contains a mantle-pad and micro-lure (Figures 7, 9-14).

The mantle-pad is a folded and articulated portion of the

mantle, and the micro-lure is a modified and innervated

incurrent aperture papilla that moves to attract fish

hosts, seemingly mimicking aquatic insect larvae (Jones

et al., 2006; Barnhart, 2008).

Such morphological and life history specialization may

have contributed to the decline of Epioblasma species, as

changes in environmental conditions over the 19 1 and

20th centuries may have disrupted this complex life cycle.

Unfortunately, the loss of numerous taxa in the genus has

prevented a more complete understanding of the life

history and taxonomy of the group, based on modern

diagnostic methods using DNA and mantle-lure displays.

Since only 7 of the 25 species and subspecies in NA

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THE NAUTILUS, Vol. 124, No. 2

Figure 1. Distribution of Epioblasma ahlstedti (current •, historic O) and E florentina aureola (current ■ historic □) in the

Tennessee River system, USA. Also shown is the distribution of E. florentina walkeri (current A historic A) in the Cumberland River

system.

remain (Williams et ah, 1993), it is possible that

additional taxa were never identified before their extinc-

tion, while other described taxa may have been pheno-

typic variants of the same species or subspecies.

The diverse phenotypic variation within Epioblasma ,

especially the varied shell morphologies and mantle-lure

displays of females, has allowed for a more comprehen-

sive approach to understanding the taxonomy of extant

species within the group, one that includes both tradi-

tional phenotypic characters and molecular markers.

The study conducted by Jones et al. (2006) showed that

the population of Epioblasma capsaefonnis in the Duck

River, Tennessee (TN) was distinct from the population

in the Clinch River, TN and Virginia (VA), and that the

population of Epioblasma florentina walkeri in Indian

Creek, VA, a tributary to the upper Clinch River, was

distinct from the population in the Big South Fork

Cumberland River, TN and Kentucky (KY). Based on

extensive phenotypic data (e.g., shell morphology,

mantle-lures, fish host specificity) and molecular data

(e.g., mitochondrial DNA, nuclear DNA microsatellites),

these authors recommended the reclassification of the

Duck River and Indian Creek populations of Epioblasma ,

respectively. I lowever, the study did not formally describe

and provide taxonomic recognition to these populations.

Thus, the purpose of this paper is to present formal de-

scriptions and provide scientific and common names for

the new species and new subspecies of freshwater mussel

in the Tennessee River system.

Figure 2. The height (axis- A) and length of the base (axis-B)

of the shell expansion are shown. The arrows on axis-B point to

the articulation points of the posterior-ventral shell expansion

with the main body of the shell. The figure was modified from

Burch (1975) and with permission from Dr. J.B. Burch.

MATERIALS AND METHODS

Type specimens, other shell material, and collection records

for Epioblasma ahlstedti , E. capsaefonnis, E. florentina

aureola , E. florentina florentina and E. florentina walkeri

were examined at the following museums: Academy of

J.W. Jones and R. J. Neves, 2010

Page 79

Figures 3-4. 3. Holotype (OSUM 68523) of Epioblasma ahlsteclti (female), 50.7 mm long and 37.8 mm high; 4. Paratype (OSUM

82238) of Epioblasma ahlsteclti (male), 45.8 mm iong and 32.0 mm high. Photos by G. Thomas Watters.

Natural Sciences of Philadelphia, Pennsylvania (ANSP);

Carnegie Museum, Pittsburgh, Pennsylvania (CM);

Florida Museum of Natural History, University of

Florida (UF), Gainesville, Florida; Museum of Comparative

Zoology, Harvard University, Cambridge, Massachusetts

(MCZ); Ohio State University Museum of Biological

Diversity, Columbus, Ohio (OSUM); and National

Museum of Natural History, Smithsonian Institution,

Washington, D.C. (USNM) [see Jones (2004) for all

examined lots]. Type specimens provided standard

references for comparing shell material from various

rivers, and collection records were used to construct

species distributions. Museum specimens of E. ahlsteclti

were identified using only female shells.

To assess differences in the shell expansion of adult

female shells among populations, simple linear regres-

sion equations of total length (x-axis) versus the height

((/-axis) of the shell expansion were computed for each

population. The height of the shell expansion was

measured from its base, which is the length between

the two articulation points with the main body of the

shell (Figure 2). Digital calipers were used to measure

shell dimensions to the nearest 0. 1 mm. To test for

differences, the slopes of the fitted-lines of each

regression equation were compared among populations

using the homogeneity of regression coefficients test

statistic.

Fecundity was estimated by counting the number of

glochidia from each of 6-10 females per population.

Although not a diagnostic trait in this study, it helped to

demonstrate quantitative differences among species.

Live female mussels for fecundity analysis were col-

lected from the following river locations: (1) E. ahlsteclti ,

Duck River, Lillard Mill [River Kilometer (RKM) 2S7.7],

Marshall County (Co.), TN; (2) E. capsaeformis , Clinch

River between Horton Ford (RKM 321) and Swan

Island (RKM 277), Hancock Co., TN; (3) E. florentina

aureola , Indian Creek, a tributary to the upper Clinch

River at R K M 518.2, Tazewell Co., Virginia (VA);

(4) E. f. walked, Big South Fork Cumberland River,

Station Camp Creek, Scott Co., TN, downstream to

Bear Creek, McCreary Co., KY (Jones et al. 2006).

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THE NAUTILUS, Vol. 124, No. 2

Figures 5-6. 5. Holotype (OSUM 82239) of Epioblasma florentina aureola (female), 44.1 mm long and 34.8 mm high; 6. Paratype

(OSUM 82240) of Epioblasma florentina aureola (male), 48.1 mm long and 33.4 mm high. Photos by G. Thomas Watters.

Fecundity was compared using analysis of variance

(ANOVA). All statistical analyses of shells and glochidia

were conducted in MINITAB 14 Statistical Software

(Minitab, Inc., State College, PA).

Samples of mantle tissue from live mussels were

collected from the above river locations and, additionally,

individuals of E. torulosa rangiana were collected

from the Allegheny River, Venango Co., Pennsylvania

(PA) (Jones et ah, 2006). Other subspecies were not

included in the study because they are presumed extinct,

i.e., E. florentina florentina , E. florentina curtisi , and

E. t. torulosa. A small piece of mantle tissue (20-30 mg)

was collected non-lethally from 8-20 live mussels from

each population (Naimo et ah, 1998).

Sequences of three regions of mitochondrial DNA

(mtDNA) and one region of nuclear DNA (nDNA) were

amplified by polymerase chain reaction (PCR) using

primers and conditions reported in: (1) 16S , ribosomal

RNA (Lydeard et ah, 1996) (2) ND1, first subunit of

NADI I dehydrogenase (Buhay et ah, 2002; Serb et ah.

2003), (3) cytochrome-b (Merritt et ah, 1998; Bowen and

Richardson, 2000), and (4) ITS-1 (King et ah, 1999). All

PCR products were sequenced with a Big Dye Termina-

tor Cycle Sequencing kit with AmpliVhq DNA Polymer-

ase (Applied Biosystems). Cycle sequence reactions

were purified using a Qiagen DNA Purification kit

(Qiagene), and subjected to electrophoresis and

sequencing using an Applied Biosystems 3100 auto-

mated sequencer [detailed PCR methods are available

in Jones (2004) and Jones et ah (2006)].

Phylogenetic analysis of DNA sequences and mor-

phological characters were conducted to infer genealog-

ical relationships among Epioblasma spp. Sequences

from mtDNA and nDNA were combined, and six mor-

phological characters (Table 1) were included in the

character matrix for a total evidence analysis (Kluge,

1989). DNA sequences were edited and aligned using

the program SEQUENCHER (version 3.0, Gene

Codes Corporation), and phylogenetic analysis was per-

formed using PAUP* (version 4.0bl0, Swofford, 1998).

J.W. Jones and R.J. Neves, 2010

Page 81

Figures 7-14. Mantle-pad displays of female Epioblasma ahlstedti , E. florentina aureola and congeners. 7. Mantle-pad and micro-

lure of E. ahlstedti. Duck River, Marshall Co., TN. 8. Protruded shell expansion of female E. ahlstedti. 9. E. capsaefonnis mantle-

pad, Clinch River, Hancock Co., TN. 10. Double micro-lure display of E. capsaefonnis ; 11. E. florentina aureola mantle-pad. Clinch

River, Tazewell Co., VA. 12. Micro-lure of E. florentina aureola. 13. E. florentina walked mantle-pad and micro-lure, Big South Fork

Cumberland River, Scott County, TN. 14. Pustuled mantle surface ofE. florentina walked. The gaps between shell valves of female

mussels are approximately 2 cm. The arrows are pointing at microlures. This figure was previously published in Jones et al. (2006) but

updated in this study to include the new species and new subspecies scientific names; photograph in Figure 9 has not been previously

published. Photographs of the mantle-pad display of E. torulosa rangiana are available in Jones (2004).

Page 82

THE NAUTILUS, Vol. 124, No. 2

Table I. Matrix and coding for shell and mantle-lure

characters for Epioblasma species. Character states were

determined from direct observation and from those reported

in Jones et al. (2006). A gap ( — ’) indicates the character was not

applicable to the species.

CHARACTER MATRIX

CHARACTERS:

(1) Prominent posterior- ventral shell expansion of adult

female. 0=absent or diminutive; l=present.

(2) Denticulations present along margin of posterior-ventral

shell expansion. 0=absent; 1 =present.

(3) Periostracum color and ray pattern. 0=yellow-green

periostraeum with irregularly spaced green rays;

l=honey-yellow periostracum with line green rays

evenly spaced over entire shell surface; 2=brown

periostracum with irregularly spaced green rays.

(4) Mantle-pad color. 0=dark purple to slate gray; l=blue to

bluish-white; 2=gray with mottled black background;

3=brown with mottled tan background; 4=white.

(5) Mantle-pad texture. 0=spongy; l=smooth; 2— pustules.

(6) Mantle-pad pustules. 0=rounded; l=pointed.

(7) Number of micro-lures prominently displayed. 0=0;

1=1; 2=2.

(8) Mantle-pad is invaginated where it meets incurrent aper-

ture. 0=yes; l=no; 2=incomplete.

Phylogenetic trees were evaluated using the maximum

parsimony (MP) criterion because the extent of

sequence divergence was low among in-group taxa (Nei

and Kumar, 2000; Felsenstein, 2004). Characters were

treated as unordered and of equal weight for the analysis

due to in-group taxa being closely related (Nei and

Kumar, 2000). The tree search was conducted using

the branch-and-bound method with ACCTRAN and

TBR options; insertions and deletions were treated as

missing data. Bootstrap analyses (10,000 replicates) were

conducted using the FAST step-wise addition option of

PAUP* to assess support for the individual nodes of each

phylogenetic tree (Felsenstein, 1985). An additional phy-

logenetic analysis was conducted using Bayesian infer-

ence in MrBayes v3.0b4 (Huelsenbeek and Ronquist,

2001), where the DNA and morphological data sets

were combined following the approach of Nylander et al.

(2004). MrBayes was run for I million generations,

sampling trees every 100 generations and posterior prob-

abilities were computed after a burn-in of 40,000 genera-

tions. In-group taxa were E. ahlstedti, E. capsaeformis,

E. florentina aureola , E. florentina walkeri , and E. torulosa

rangiana. Because of significant differences in morphol-

ogy and DNA sequences, the Cumberland Combshell

(Epioblasma brevidens ) and Snuffbox (Epioblasma

triquetra) were designated as out-group taxa. The study

by Jones et al. (2006) showed that DNA sequences from

these two species are diverged from the in-group taxa

by ~5%, and based on obvious differences in shell mor-

phology, Johnson (1978) classified E. brevidens and

E. triquetra into different Epioblasma subgenera, Plagiola

and Truncillopsis , respectively. Furthermore, previous

phylogenetic studies have demonstrated the monophyly

of the Epioblasma among North American unionids

and that E. brevidens and E. triquetra are basal to the in-

group taxa (Campbell et al., 2005; Zanatta and Murphy,

2006). Thus, available morphological and genetic data jus-

tify use of these two species as appropriate out-group taxa.

Photographs of the mantle-pad and micro-lures of live

female mussels were taken using a Nikonos V underwater

camera with 28 or 35 mm macro-lenses and Kodak 200

Ektachrome film. Female mussels were held in tempera-

ture-controlled water in recirculating artificial streams

with gravel-filled bottoms. This setup allowed females to

display their mantle-pad and behavioral observations of

micro-lure movements to be recorded under controlled

conditions [photographic methods were previously

published in |ones et al. (2006)].

Epioblasma ahlstedti new species

Duck River Dartersnapper

Figures 3, 4, 7, 8

Diagnosis: The following diagnostic morphological

characteristics of Epioblasma ahlstedti are based on the

female and are summarized in Table 2: (1) pronounced

posterior-ventral shell expansion of the adult shell;

(2) slate-gray to dark purple mantle-pad; (3) spongy tex-

ture of the mantle-pad; and (4) display of a single,

tan-colored micro-lure that moves slowly side-to-side. In

young individuals, the base of the shell expansion is con-

stricted, appearing narrow but distinctly protruded. How-

ever, as the female shell grows, the shell expansion

becomes extremely protruded and enlarged, compared to

the main body of the shell. The shell expansion of

E. ahlstedti is distinguishable from that of E. capsaeformis

using the following criteria: (1) length of the shell expan-

sion base in young individuals (~3-5 y), ranging in size

from ~35-45 mm, typically appears constricted, being

~5-10 mm narrower basally than those of female

E. capsaeformis of similar age and size, and (2) mean

height (9.6 mm) and maximum height (24.6 mm) of the

shell expansion of adult females is significantly greater

than that of female E. capsaeformis (Table 3; Figure 15).

Description: Length of the female shell can reach

60 to 70 mm, with mean length ~42 mm (Table 3). Male

shell lengths are similar. The shell outline of males is

typically elliptical, appearing pointed at the posterior

end (Figure 4), whereas the shell outline of females is

more sub-oval and rounded, with a veiy enlarged and

protruded posterior-ventral shell expansion (Figures 3, 8).

The mean height of the shell expansion of the female is

~10 mm or ~23% of shell length, but maximum height is

J.W. Jones and R. J. Neves, 2010

Page S3

Table 2. Diagnostic morphological and molecular genetic characters for Epioblasma alilstedti , E. florentina aureola and closely

related taxa. Data are summarized from Jones et al. (2006).

Table 3. Mean shell length, mean height of shell expansion, and linear regression equations of shell expansion height (y- axis) to

total length (x-axis) of adult female mussels. Pairwise comparisons of regression equation slopes were significantly different

(p<0.001), except equations A vs D, and C vs D. *The p -value indicates the significance level of the slope for each regression

equation.

~25 mm (Table 3), and it is dark green, sometimes

appearing almost black. Denticulations occur along the

margin of the shell expansion and are typically ~0.5 to

1 mm long and spaced ~0.5 to 1 mm apart. The

periostracum of adults is yellowish green, becoming more

yellowish at the anterior end. The shell surface contains

distinct broad to fine green rays that are typically irregu-

larly spaced. The male shell is short and high with a

shallow sulcus. Nacre color is white, but hues of blue

and salmon may be present, especially near the beak

cavities.

The color of the foot and gills of E. ahlstedti is dull

white. In females, only the two outer gills are marsupial

(i.e., the outer water-tubes contain and brood glochidia

when gravid). Located at the distal end of each marsupial

water-tube is a pore, which allows for release of glochidia.

The mantle-pad is slate-gray to dark purple and has a

spongy texture, and the micro-lure is tan (Figure 7). The

posterior portion of the mantle-pad is invaginated where

it meets the incurrent aperture, so the attachment points

of the micro-lures cannot be seen when the female is

displaying (Jones et al., 2006).

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THE NAUTILUS, Vol. 124, No. 2

30

03035404550566065 70

Figure 15. Relationship of posterior-ventral shell expansion height versus shell length of female Epioblasma ahlstedti and

E. capsaeformis, and of female E. florentina aureola and E. florentina walked. Pairwise comparison of regression equation slopes

was significantly different (p<0.001) between Epioblasma ahlstedti and E. capsaeformis but not significantly different between

E florentina aureola and E. florentina walked. However, the slope of each regression equation is significant lor all four taxa

(see Table 3).

Type Material: Holotype: Designated herein as

OSUM 68523, collected by 11.15. Athearn, from type local-

ity, 30 Sep. 1956. Paratypes: CM 61.1 1669, Duck River,

Lillard Mill, Marshall Co., TN, collected by A.E. Ortmann,

25 Aug. 1923; MCZ 236214, Duck River, Lillard Mill,

Marshall Co., TN, collected by H.D. Athearn, 30 Sep.

1956; OSUM 52509, Duck River, Lillard Mill, Marshall

Co., TN, collected by S.A. Ahlstedt, I Oct. 1982; OSUM

82238, Duck River, Lillard Mill, Marshall Co., TN, col-

lected by S.A. Ahlstedt, I Oct. 1999 (see Appendix for

other material examined); OSUM 82241, Duck River,

Lillard Mill, Marshall Co., TN, collected by H.D. Athearn,

30 Sep. 1956.

Type Locality: Duck River, Lillard Mill, Marshall Co.,

TN, 35°35'09.08" N; 86°47' 14.07" W.

Comparison with Similar Species: The shell of adult

Epioblasma capsaeformis (. sensu stricto ) in the Clinch

River is of small to medium length (~30-50 mm). The

shell surface contains distinct broad to line green rays

that are irregularly spaced, and veiy similar to those of

E. ahlstedti. However, the following diagnostic, morphol-

ogical characteristics of female E. capsaeformis distin-

guish it from E. ahlstedti: (1) bluish-white mantle-pad

(Figure 9), (2) smooth texture of the mantle-pad, and

(3) simultaneous display ol two micro-lures that move

J.W. Jones and R.J. Neves, 2010 Page 85

Table 4. Fecundity estimates of female Epioblasma.

Mean number ol

*Mean fecundity for Epioblasma ahlstedti is significantly different (p<0.05) from the other taxa.

synchronously in a circular motion; the left micro-lure

moves clockwise, and the right micro-lure moves coun-

terclockwise (Figure 10). The dorsal margin of the man-

tle-pad is black, forming a discrete uniform band

~2— 3 mm wide. The posterior portion of the mantle-pad

is not invaginated where it meets the incurrent aperture,

so the attachment points of the micro-lures can be seen

when the female is displaying. The dentieulations along

the margin of the shell expansion of E. capsaeformis

are typically finer and more closely spaced than those

of E. ahlstedti. The shell expansion is greenish, but not as

dark as that of E. ahlstedti.

Life History: The typical habitat of E. ahlstedti is

gravel shoals in medium to large rivers. It is a long-term

brooder, gravid from late summer to the following spring

and early summer. In the Duck River, at least some

females will emerge from the substrate in early spring

(e.g., Mareh-April) to display their mantle-pad lure to

attract host fishes, while others emerge later in the

spring and summer (e.g., May-July). Mean fecundity of

females was 18,757 glochidia, and ranged from 6,668 to

38,716 (Table 4). The largest females were not examined;

hence maximum fecundity is unknown but likely exceeds

50,000 glochidia. Known fish hosts for E. ahlstedti

include three darter species, the greenside darter

(Etheostoma hlennioides), fantail darter ( Etheostoma

flabellare ), and redline darter ( Etheostoma rufilineatum)

(Jones et ah, 2006). However, tested hosts were not col-

lected from the Duck River, but from the North Fork

Holston River, VA, in the upper Tennessee River drain-

age. Although all three darters are widely distributed and

common in Duck River, the native Duck River hosts

remain uncertain.

Molecular DNA Markers anti Phylogenetic Analysis:

The Duck River population of E. ahlstedti contains pre-

sumably diagnostic nucleotides at three mitochondrial

DNA gene regions [16S (n= 1), cytochrome-b (n— 4), and

ND 1 (n=2)] and at one non-coding nuclear DNA region

[ITS-] (n=2)] (Table 2). Rased on analysis of 10 nuclear

DNA microsatellite loci, the population is moderately

diverged (FST=0.12) from the Clinch River population of

E. capsaeformis (Jones et ah, 2006). The MP and Rayesian

phylogenetic analyses showed high statistical support lor

the E. ahlstedti clade (Figures 16, 17); a finding previously

demonstrated by Jones et al. (2006) using only the DNA

sequences. Furthermore, die MP tree in Jones et al. (2006)

shows E. ahlstedti as the basal member of the in-group taxa,

whereas the MP tree (Figure 16) reported in this study

shows E. tomlosa rangiana as basal. However, several inte-

rior nodes in both MP trees are weakly supported and

collapse in the respective consensus trees (not shown). A

50% majority-rule Bayesian consensus tree depicting a

more conservative topology is given in Figure 17.

Distribution: Epioblasma ahlstedti is currently

restricted to 48.3 RKM in the Duck River from Lillard

Mill (RKM 286.5) downstream to the backwaters of the

Old Columbia Dam reservoir (RKM 238.2) in Marshall

Co. and Maury Co., west-central Tennessee (Figure 1).

Based on shells, the species likely occurred historically in

the Buffalo River, TN (Parmalee and Bogan, 1998), a

tributary to the Duck River, and the Tennessee River at

Muscle Shoals and Shoal Creek, Lauderdale Co., AL

(Jones, 2004).

Conservation Status: The oyster mussel ( Epioblasma

capsaeformis) was listed as endangered under the Endan-

gered Species Act (ESA) in 1997, to include the Duck

River population. Now that E. ahlstedti has been designated

a separate species, it is restricted to only the Duck River

population. Being linearly distributed to 48 river kilome-

ters and susceptible to a stochastic impact, this species

should be considered critically endangered and continue

to receive full protection under the ESA.

Etymology: The species name is given in honor ol

biologist Steven A. Ahlstedt, U.S. Geological Survey

(retired), Knoxville, TN, who has dedicated over 30

years of sendee to freshwater mussel conservation in

the United States. The common name denotes the

snapping behavior of many female Epioblasma species

(i.e., displaying females wall quickly close their shells

when touched, which can capture a host fish to facili-

tate infestation with glochidia on the host) ( Jones et al.,

2006).

Epioblasma florentina aureola new subspecies

Golden Riffleshell

Figures 5, 6, 11, 12

Diagnosis: The following diagnostic morphological

characteristics of E. florentina aureola are based on the

female and are summarized in Table 2: (1) gray mantle-

pad with a black mottled background, and (2) mantle-

pad has rounded pustules.

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THE NAUTILUS, Vol. 124, No. 2

E. capsaeformis 1 (A/=4)

E. capsaeformis 2 (AM)

E. capsaeformis 5 (A/=1)

E. capsaeformis 6 (AM)

E. capsaeformis 3 (N=2)

E. capsaeformis 4 (AM)

E. fiorentina aureola 1 (N=5)

E. fiorentina aureola 2 (A/=1)

E. fiorentina walkeri 1 (AMO)

E. fiorentina walkeri *

E. ahlstedti 1 (A/=9)

E. ahlstedti 2 (AM)

E. torulosa rangiana 1 (AM)

E. torulosa rangiana 2 (A/=3)

E. torulosa rangiana 3 (A/=2)

E. triquetra (AM)

E. brevidens (AM)

Figure 16. Cladogram showing phylogenetic relationships among Epioblasma ahlstedti , E. fiorentina aureola and congeners,

inferred from the combined mitochondrial DNA regions of 16'S (468 bp), cytochrome-b (360 bp), A’/J I (568 bp), the nuclear DNA

region ITS-1 (515 bp) and eight morphological characters (see Table 1) using maximum parsimony (MP) (31 equally parsimonious

trees were resolved; length=195 steps; 0=0.92; RI=0.89). Numbers above the branches (MP) represent bootstrap support (10,000

replicates); only values >50% are shown. All E. fiorentina walkeri were identical; however, to demonstrate the monophyly of this

population, an additional sequence was added to the analysis. Out-group taxa are E. triquetra and E. brevidens.

Description: Length of the female shell can reach

46 mm in Indian Creek and the upper Clinch River, with

mean length of 40 mm (Table 3). Shell lengths of males

are similar. The shell outline of females is sub-oval and

rounded with a moderately protruded shell expansion

(Figure 5). The mean height of the female shell expan-

sion is 5.7 mm or ~14% of shell length, but maximum

height can reach ~10 mm (Table 3; Figure 15). Dentic-

ulations occur along the margin of the shell expansion

and are fine and narrowly spaced ~0.5 mm apart. The

shell outline of males is elliptical, appearing pointed at

the posterior end (Figure 6), and may have a shallow

sulcus, especially older individuals. The periostracum of

adults can range from golden honey-yellow, to tan and

J.W. Jones and R. J. Neves, 2010

Page 87

Figure 17. Phylogenetic relationships. 17. A 50% majority-rule consensus tree (phylogram) showing phylogenetic relationships

among the ingroup taxa. The tree was produced from the same DNA sequences and morphological characters listed above and

evaluated using Bayesian inference. The analysis was run for 1 million generations with a burn-in of 40,000 generations (mean log

likelihood=-3,667). Numbers at the nodes are calculated posterior probabilities (>50%) indicating proportion of trees containing the

inferred nodes. Numbers in parentheses at the end of each taxonomic name represent the number of observed DNA haplotypes. * All

E. florentina walkeri haplotypes were identical; however, to demonstrate the monophyly of this population, an additional sequence

was added to the analysis. Out-group taxa are E. triquetra and E. hrevidens.

brown, but coloration is usually evenly distributed over

the shell, although occasionally the shell expansion of the

female is tinted green. The periostracum contains distinct

fine green rays that are evenly spaced over the shell. Nacre

color is white, but hues of blue and salmon may be present.

The color of the foot and gills of E. florentina aureola

is dull white. In females, only the two outer gills serve as

marsupia. Each marsupial water-tube contains a distal

pore to allow for release of glochidia. The mantle-pad

is gray with a black-mottled background and with

rounded pustules (Figures 11, 12). The dorsal margin

of the mantle-pad is tan, forming a discrete, uniform

band ~2-3 mm wide. Micro-lures are darkly colored,

and only a single micro-lure is prominently displayed.

Page 88

THE NAUTILUS, Vol. 124, No. 2

which moves slowly side-to-side in a sweeping motion

(Figure 12). The posterior portion of the mantle-pad is

invaginated where it meets the incurrent aperture, so

attachment points of the micro-lures cannot he seen

when the female is displaying. The undisplayed

microlure is obscured from view inside the invaginated

area of the mantle pad (Figure 12).

Type Material: Holotype: Designated herein as

OSUM 82239, collected by Leroy Koch, from type local-

ity, 1 Sep. 1998. Paratypes: OSUM 16266, Clinch

River, Route 460 Bridge, Cedar Bluff, Tazewell Co., VA,

collected by D.H. Stansbery and J.f. Jenldnson, 6 Oct.

1965; OSUM 42321, Clinch River, Route 460 Bridge,

Cedar Bluff, Tazewell Co., VA, collected by C.R. Ciola,

I July 1978; OSUM 42434, Clinch River, below railroad

bridge. Cedar Bluff, Tazewell Co., VA, collected by C.R.

Ciola and G. Wargowsky, 10 Aug. 1978; OSUM 43294,

Clinch River, below railroad bridge. Cedar Bluff, Tazewell

Co., VA, collected by J.M. Condit and C.R. Ciola, 15 July

1978; OSUM 53252, Clinch River, Cedar Bluff, Tazewell

Co., VA, collected by R. Taylor, 10 July 1983; OSUM

82240, Clinch River, Route 460 Bridge, Cedar Bluff,

Tazewell County, VA, collected by Leroy Koch, I Sep.

1998. (See Appendix for other material examined.)

Type Locality: Clinch River, Route 460 Bridge,

Cedar Bluff, Tazewell County, VA, 36°05/16.13,/ N;

81°46'05.98" W.

Comparison with Similar Species: The shell of adult

E. florentino walked ( sensu stricto ) in the Big South

Fork Cumberland River is of small to medium length

(~30-45 mm) (Table 3), and nearly indistinguishable in

shape and color to those of E. florentina aureola. The

mean height (8.5 mm) and maximum height (14.1 mm)

of the shell expansion of adult females is slightly

larger than that of female E. florentina aureola , but it

is not significantly greater (Table 3; Figure 15). The

periostracum color of both is honey-yellow, to tan and

brown, with fine green rays evenly spaced across the

shell. However, the following diagnostic morphological

characteristics of female E. florentina walked distinguish

it from E. florentina aureola-. (1) mantle-pad is brown

with a tan-mottled background (Figure 13); and (2) while

the mantle-pad also is pustuled, the pustules are pointed

and not rounded (Figure 14). The denticulations along

the margin of the shell expansion of the female shell are

larger and more widely spaced ~1 mm apart, compared

to those of E. florentina aureola. Similarities include

display of a single micro-lure, which moves slowly side-

to-side, and the dorsal margin of the mantle-pad is tan,

forming a distinctive band ~2-3 mm wide. Similarly the

posterior portion of the mantle-pad is invaginated where

it meets the incurrent aperture, so the attachment points

of the micro-lures cannot be seen when the female is

displaying.

Life History: The typical habitat of E. florentina aure-

ola is stable sand and gravel substrates in headwater

reaches of rivers and creeks. The subspecies is a long-term

brooder, gravid from late summer to the following spring

and early summer (Rogers et al., 2001). In Indian Creek,

females will emerge in spring and summer (April-July)

to display their mantle-pad lure to attract host fishes.

Based on an estimate from a single female, maximum fe-

cundity is at least 20,000 gloehidia (Rogers et ah, 2001).

However, mean fecundity based on six females during

this study was 7,602 gloehidia per female, ranging from

3,261 to 12,558 gloehidia (Table 4). Known fish hosts for

E. florentina aureola based on laboratory trials include:

greenside darter ( Etheostoma blennioides) , fantail darter

(£. flabellare ), redline darter (E. nifilineatum), snubnose

darter (£. simoterum), black seulpin ( Coitus baileiji ), mot-

tled sculpin (C. bairdi), and banded seulpin (C. carolinae )

(Jones and Neves, 2001; Rogers et ah, 2001).

Molecular DNA Markers ancl Phylogenetic Analysis:

The Indian Creek and upper Clinch River population

of £. florentina aureola contains presumably diagnostic

nucleotides at two mitochondrial DNA gene regions [cyto-

chrome-b (n=l), and ND1 (n=l)] (Table 2). Further,

based on analysis of 10 nuclear DNA microsatellite loci,

the population is diverged (Est=0.39) from the Big South

Fork Cumberland River population of £. florentina

walked (Jones et ah, 2006). The MP and Bayesian phylo-

genetic analyses showed high statistical support for the

£. florentina aureola clade (Figures 16, 17), a finding

previously reported by Jones et ah (2006).

Distribution: Epiobla.sma florentina aureola is cur-

rently restricted to the lower ~1.6 KM of Indian Creek

in southwestern Virginia (Figure 1). Historically, this sub-

species presumably occurred in numerous tributary

streams of the middle and upper Tennessee River system

downstream to the Duck River. However, all of these

historical populations are considered extirpated. There-

fore, the color and texture of the mantle pad and other

traits of those populations are unknown. Thus, it is

unknown whether these historical populations repre-

sented £. florentina aureola or other undescribed taxa.

Conservation Status: The Tan Riifleshell (£. florentina

walked) was listed as endangered under the ESA in 1977.

Now that £. florentina aureola has been designated herein

as a separate subspecies, the subspecies only occurs as a

single small population in the lower reach ot Indian

Creek, VA. This subspecies is one of the most critically

endangered populations of freshwater mussel in the

United States being linearly distributed to a short stream

section and highly susceptible to a stochastic event. This

subspecies should continue to receive maximum protec-

tion under the ESA.

Etymology: The subspecies name aureola is the

diminutive form of the Latin adjective for golden, and is

here chosen to denote the honey-yellow to occasionally

golden color of the shell.

Remarks: The anatomical characteristics of females,

such as the distal pores, mantle-pad, and micro-lure.

|.YV. (ones and R.J. Neves, 2010

Page 89

and the shell expansion with denticulations along the

margin of the shell are considered advanced traits among

unionids, based on their complexity and uniqueness to

Epioblasma (Jones et ah, 2006). the prominent shell

expansion of female E. ahlstedti is a defining trait first

recognized around the turn of the 20th century by the

American malacologist Bryant Walker (1856-1936). The

following undated letter was written by him and found in

a small box in the ANSP shell collection (ANSP 100538).

The letter was a hand-written note to a physician and to

our knowledge has never been published. The hand-

writing was difficult to read but was deciphered exactly

as is by JWJ, with assistance from Paul Callomon, Elana

Benamy, and Earle Spamer of ANSP, on 8 Jan. 2003:

“I also send some Truncillas [ Epioblasmas ] that

may be of interest. The Shoal Creek form is typical

capsaeformis as I understand it. The male of the

Duck R. form is very similar, but the females

have invariably the enormous expansion of the

specimen sent. In the Clinch, on the other hand,

the females are quite typical in form, but the males

are usually decidedly more elongated. The Duck

R. form has been generally called "turgidulus" but

it is not. Lea’s turgidulus is the male of deviata as I

proved to my own satisfaction, at least, while I was

in Washington.”

“P.S. The element of uncertainty in capsaeformis

matter is the fact that we don’t know what the $

form of the Cumberland is. The $ shell I had at

Phila. & which agreed best with Leas figure ol the

type was from the Duck R., variety expansa. The

only Cumberland R. $ I have seen is an immature

shell belonging to Ferris, and it is apparently like

the Tenn. R. & Shoal Crk. form. It the 9 Cumber-

land R. form is expansa like the Duck R. shell, that

would be typical capsaeformis & expansa could

not be used”.

These observations by Bryant Walker indicate that the

taxonomic position of the Duck River population was

being questioned nearly 100 years ago, and that the

expansion of the female shell was seen as a diagnostic

trait when compared to specimens collected from other

rivers in the region, including shells from the Clinch

River. In Walker’s view, the size of the shell expansion

of adult females is a signature phenotypic character,

reaching a mean and maximum height that is greater

than those of other species and subspecies belonging

to the Epioblasma subgenus Tondosa [sensu Johnson

(1978)]. Thus, the combination of key phenotypic traits,

especially the unique shell morphology and mantle-lure

display of females, unambiguously define E. ahlstedti as

a valid species.

The population of Epioblasma florentina aureola

in the upper Clinch River watershed is not deserving

of a separate species designation because of several

shared traits with E. florentina walkeri in the Big South

Fork Cumberland River: (1) honey-yellow to tan-

colored periostracum, (2) similar fish host specificity,

(3) pustuled mantle-pads, and (4) preference for head-

water stream habitats. These two populations also have

similar-sized gloehidia, similar fecundity, and are

closely related phylogenetically. In addition, the

periostracum color of the nominal species E. florentina

florentina is also yellow and was thought to simply

represent clinal variation; i.e., the large river form of

the subspecies complex. Ortmann (1918; 1924; 1925)

considered the two forms as merely clinal variants, a

claim supported by his observation that the big river

form appeared to grade into the headwater form as

one progressed upstream. However, based on the shell

material examined in Jones (2004) and Jones et al.

(2006), it is uncertain whether E. florentina florentina

merely represents clinal variation, a subspecies or per-

haps even a separate species for the following reasons:

(1) large distances of seemingly unoccupied habitat

commonly occurred between mainstem and headwater

populations (e.g.. Clinch and Holston rivers >200

RKM), and ecological conditions between mainstem

and headwater locations are substantial (e.g. distribution

of host fishes, water temperature, stream size, etc.); (2)

a transitional series of shells representing a continuously

distributed population of this species from mainstem to

headwaters does not exist ■ and (3) because most

populations are extirpated, additional genetic, morphol-

ogical and life history data are unobtainable. For exam-

ple, available specimens of E. florentina florentina

collected from the lower Clinch River near its mouth

are short (~30-35 mm), solid, and thick-shelled, and are

quite distinctive from the larger-sized headwater form E.

florentina aureola (Jones, 2004). However, because E.

florentina florentina is extinct, adequate comparisons of

the mantle-lure and DNA cannot be made with the

other subspecies. Therefore, since each nominally

described subspecies occurred or occurs in distinct geo-

graphic regions and habitats, we believe E. florentina

ssp. minimally was a polytypic species complex and best

categorized by the current trinomial designations.

The current taxonomy of Epioblasma recognizes 20

species and 5 subspecies (Turgeon et al., 1998; Williams

et al., 1993). Thus, with the description of E. ahlstedti

and E. florentina aureola , 21 species and 6 subspecies

now are recognized in the genus. The historical distribu-

tions of E. florentina aureola and E. florentina walkeri

are unclear because most populations are extirpated

and only shell material and collection records are

available to assess the distribution of each subspecies.

Furthermore, the anatomy of live individuals cannot

be compared among historical populations. Therefore, a

practical approach to delineating the distribution of

each subspecies is to consider all records of E. florentina

walkeri in the Tennessee River drainage as E. florentina

aureola , and all respective records in the Cumberland

River drainage as E. florentina walkeri. This approach

would simplify the management and recovery of each

subspecies within their respective river drainages.

Page 90

THE NAUTILUS, Vol. 124, No. 2

ACKNOWLEDGMENTS

Financial support for this project was provided by the

U.S. Fish and Wildlife Service (USFWS) and the

Tennessee Wildlife Resources Agency. We thank Brett

Ostby, Virginia Tech University, for assistance in

preparing the distribution map. We especially thank

Robert Butler, USFWS, Jim Williams, U.S. Geological

Survey (Retired), Daniel Graf, University of Alabama,

and an anonymous reviewer tor their respective peer

reviews of this work, which greatly improved the

manuscript. We also gratefully acknowledge G. Thomas

Watters and Clarissa Lawlis at the Museum of Biological

Diversity, Ohio State University for cataloging and

photographing the shell holotypes and paratypes, and

Jose H. Leal, The Bailey- Matthews Shell Museum, for

his assistance in preparing the figures. The views

expressed in this publication are the authors and do

not necessarily represent those of the USFWS.

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APPENDIX

(Continued.)

THE NAUTILUS 124(2):93-99, 2010

Page 93

New species of Bolma (Gastropoda: Vetigastropoda: Turbinidae)

from the tropical deep sea

Axel Alf

University of Applied Sciences Weihenstephan-Triesdorf

91746 Triesdorf, GERMANY

Philippe Maestrati

Philippe Bouchet

Museum National d’Histoire Naturelle

57 rue Cuvier

75231 Paris Cedex, FRANCE

ABSTRACT

Five new species of Bolma are described, three from

New Caledonia, one from Mozambique and one from French

Polynesia, all from deep reef (75-155 m) to bathyal (230-580 m)

depths. Four of the new species have been sequenced, and their

holotypes are also voucher specimens for COI sequences, thus

contributing to a new generation of name-bearing types. The

descriptions and names are provided in advance oi a forthcom-

ing shell-based revision of the genus Bolma , and in advance of a

detailed molecular- and morphology-based study ol Bolma in

New Caledonian waters.

INTRODUCTION

The gastropods of the turbinid genus Bolma Risso, 1826,

live at tropical and warm-temperate latitudes in the

Mediterranean, West African, South African, and Indo-

West Pacific biogeographical provinces; there are no

Bolma in the western Atlantic or eastern Pacific. With

the exception of the type species Bolma rugosa (Lin-

naeus, 1767), which occurs commonly near-shore to

about 200 meters deep, Bolma species are uncommon

to rare, mostly on hard bottoms between 100 and 500-

800 meters deep. Ben and Ponder (1979) revised the

Recent and fossil species, and recognized 19 valid spe-

cies (two of which with, respectively, 2 and 3 subspecies),

from among 29 nominal species. Ongoing explorations

have since added 12 more species, all from South Africa

and the Indo-West Pacific. Some of the t&xa treated by

Beu and Ponder as synonyms or subspecies have also

been re-evaluated, and the genus Bolma , with about 35

valid species, is the subject of a forthcoming monograph

by Axel Alf and Kurt Kreipl, to appear in the Concholog-

ical Iconography. The purpose of the present paper is

to describe several new species prior to the publication

of that monograph. Three of them originate from

New Caledonia, which has been intensively sampled

since the late 1970s through the Tropical Deep-Sea

Benthos program (Bouchet et al., 2008). Early in the

program, Bouchet and Metivier (1983) reported three

species of Bolma from New Caledonia, namely B. guttata

(A. Adams, 1863), B. henica (Watson, 1885), and

B. opaoana Bouchet and Metivier, 1983. Since then, the

program has been extended to other island groups in the

South Pacific and, more recently, in the Indian Ocean,

revealing still more species of Bolma. One of the new

species is thus described based on material collected from

seamounts surveyed off Madagascar in 1980, and then

again off Mozambique in April 2009. And finally, while

this paper was being put together, another very distinctive

new species was collected in September-October 2009 off

the Society/ Islands in French Polynesia.

One difficulty of Bolma systematic^ — in common with

other vetigastropods with their non-feeding short-lived

planktonic larvae — is the understanding of what consti-

tutes geographical vs. population variation (Meyer et al.

2005). In this respect, the Bolmas of New Caledonia and

the Solomon Islands have been the subject of molecular

work by Magalie Castelin, as part of her Ph.D. thesis, the

results of which wall be reported elsewhere. The purpose

of the present paper is also to provide names and facilitate

the presentation and discussion of this molecular work.

Abbreviations and Text Conventions: lv, live-taken

specimen; dd, empty shell; stn, station; MNHN, Museum

National d’Histoire Naturelle, Paris, France; NMNZ,

Museum of New Zealand Te Papa, Wellington, New

Zealand; NMP, Natal Museum, Pietermaritzburg, South

Africa; ZRC, Raffles Museum, Zoological Reference Col-

lection, National University, Singapore.

SYSTEMATICS

Family Turbinidae Rafinesque, 1815

Genus Bolma Risso, 1826

Type Species: Turbo rugosus Linnaeus, 1767 (by

monotypy).

Bolma castelinae new species

(Figures 1-7)

Description: Shell of average size for genus, trochoid

with straight sides, as tall as wide, spire angle about 75°,

Page 94

THE NAUTILUS, Vol. 124, No. 2

rather thin-shelled and light. Teleoconch of 6% whorls,

first two planispiral, subadult and adult whorls convex

with angular peripheral cord overhanging narrow, flat,

subsutural ramp, giving the impression of deep suture.

Basal cord delimiting distinct basal disc. Sculpture

consisting of beaded spiral cords, number of cords in-

creasing from single subsutural cord above periphery on

third whorl, to 3 on last 3 whorls, and with 3 additional

secondary cords on last 1/3 whorl behind aperture;

strong peripheral and weaker basal cords bearing short,

scaly spines; space between peripheral and basal cords

almost vertical, overall smooth except for one cord bear-

ing short, scaly spines; base smooth, polished. Columella

smooth and evenly rounded, thickened, but basal callus

indistinct. Aperture oval, outer lip sharp in holotvpe

(expanded in fully adult specimens). No umbilicus.

Background color pinkish salmon, beads, adapertural

side of spines, and interspace between peripheral and

basal cords lighter, base porcellaneous white; columella

white and nacreous, aperture nacreous within. Opercu-

lum thick, convex, smooth, white. Dimensions of holo-

type: height 25.2 mm, diameter 25.1 mm. Adults may

reach a height of 30 mm, diameter 28 mm.

Holotype: MNHN 22823 (lv).

Paratypes: I, MNHN 22824 [Ebisco, stn CP2579,

20°2T S, 158°40' E, 440-455 m, I Oct. 2005]; 1, MNHN

22840 [Halical 1, stn DW02, 18°54' S„ 163°24' E, 352-

397 m, 23 Nov. 1994]; 1, ZRC.MOL.2954 [Smib 4, stn

DW34, 24° 55' S, 168°22' E, 515 m, 7 March 1989];

1, NMNZ M. 297232 [Smib 4, stn DW34],

Material Examined and Distribution: More than

60 lots, until several hundred live-talcen specimens and

empty shells, from the Norfolk Ridge, mainland New

Caledonia off lie des Pins, Grand Passage between main-

land New Caledonia and Recifs d’Entrecasteaux, and

banks on Lord Howe Ridge, alive at depths between

350 and 580 meters. Not found during research cruises

to the Solomon Islands, Vanuatu, or Fiji.

Type Locality: South of New Caledonia: Norfolk

Ridge, Kaimon Mam Bank, 24045, S, 168°06; E, 600-

896 m [Norfolk 2, stn DW 2091],

Remarks: Tl iroughout their range, populations of

Bolma castelinae are remarkably stable in shape and

sculpture, and do not show geographical or bathymetri-

cal variation. In Magalie Castelin’s molecular tree (pers.

comm.), B. castelinae is nearest to a possibly new species

from the Solomon Islands tentatively identified by us as

B. cl. bartschii (Dali, 1913). The latter has a peripheral

cord with fewer, stronger spines, overhanging a broader,

concave subsutural ramp; the spiral cords are broad,

with narrow interspaces; and the basal disc is sculptured

with headed cords and bears a thin callus. Of the species

present in New Caledonia, B. castelinae most resembles

B. recens (Dell, 1967), but molecular analyses have con-

firmed that they are distinct. B. castelinae always has

3 rows of short scaly spines on the middle part of the last

whorl: one on peripheral and basal angles and one

between them, and a smooth and glossy base. In

B. recens, the central row of spines is weak or absent,

and flanked by numerous spiral grooves, and the basal

disc is sculptured with concentric cords.

Etymology: The species is named after Dr (Ms)

Magalie Castelin, whose molecular work has resulted in

robust species delimitations in the genus Bolma.

Bolma pseudobathyraphis new species

(Figures 8-14)

Bolma guttata — Bouchet and Metivier, 1983: 10, figs. 4-6

[not figs. 7-8, which represent B. fuscolineata Alf and

Kreipl, 2009] .

Description: Shell large for genus, trochoid with veiy

convex whorls, taller than wide, spire angle about 75°,

rather thin shelled and light. Teleoconch of 7 to 714

whorls, first 2 whorls planispiral, next 3 rather flat-sided,

last two strongly convex with narrow, flat, subsutural

ramp and overhanging peripheral cord, giving impres-

sion of a veiy deep, channelled suture. Periphery and

basal cords weakly delimited, peripheral cord bearing

row of short to very short, triangular, scaly spines which

become evanescent near the peristome. Sculpture of

fine, prosocline, axial lamellae extending on spire as well

as on base, and strong, beaded spiral cords; on third

whorl, single subsutural cord above periphery number

increasing to 4 on penultimate whorl, and to 7 on last

whorl; space between peripheral and basal cords with

three cords, central one stronger, bearing short scaly

spines; base with 5 beaded cords. Columella smooth

and evenly rounded, basal callus thick around columellar

margin, thin on basal disc. Aperture oval, outer lip

expanded, but not flaring, in adult specimens. No umbi-

licus. Background color light brown or light purple, occa-

sionally more white or pink, distinctly darker above

periphery, and with or without small, purple-brown spots

between the beads on spire as well as on base. Columella

white and nacreous, aperture nacreous within. Opercu-

lum thick and heavy, oval with convex, sometimes wrin-

kled, surface, white. Dimensions of holotype: Height

42 mm, diameter 37.5 mm, operculum largest diameter

17.1 mm.

Holotype: MNHN 22825 (lv).

Paratypes: 1, MNHN 22826, same locality as holo-

type; E ZRC.MOL.2955 [Smib 4, stn DW65, 22° 55' S,

167° 15' E, 400-420 m, 10 Mar. 1989]; 1, NMNZ

M. 297233 [Smib 2, stn DW6, 22°56' S, 167°16' E, 442-

460 m, 17 Sep. 1986].

Material Examined and Distribution: Bolma

pseudobathyraphis is the most abundant Bolma species

in New Caledonia, with about 200 lots comprising ca.

1000 live-taken specimens and shells, from the Norfolk

Ridge, mainland New Caledonia off lie des Pins, Grand

Passage between mainland New Caledonia and Recifs

d’Entrecasteaux, banks on Lord Howe Ridge, and the

A. Alfetal.,2010

Page 95

Loyalty Ridge, alive at depths between 240 and

530 meters. Not found during research cruises to the

Solomon Islands, Vanuatu or Fiji.

Type Locality: Norfolk Ridge, south of New Caledo-

nia, 23°42' S, 168° 16' E, 377 m [Norfolk 2, stn CP2050,

24 Oct. 2003]

Remarks: Bolma pseudobathijraphis is very stable in

shape, sculpture and size, except on Lord Howe Ridge

where there exists a morph with long spines on the

periphery (Figure 14), which however is not molecularly

distinct.

Rouchet and Metivier (1983) had assigned their New

Caledonia material to Bolma guttata (A. Adams, 1863),

because of its superficial resemblance to the Indian

Ocean populations described as Bolma bathyraphis

(E.A. Smith, 1899), treated by Ben and Ponder (1979) as

a subspecies of B. guttata. However, B. pseudobathijraphis

differs from B. bathyraphis by its veiy convex whorls and

deep suture, and a spiral sculpture of spiny, rather than

rounded, beads. Juveniles of B. pseudobathijraphis also

superficially resemble B. fuscolineata Alf and Kreipl,

2009, and had been confused with it by Bouchet and

Metivier (1983), but they differ by their much higher last

whorl and aperture, more widely spaced peripheral and

basal cords, and more uniform color pattern (Figures 11-

12 vs. 15-16).

In Magalie Castelin’s molecular tree, Bolma

pseudobathijraphis is nearest to to B. millegranosa

(Kuroda and Habe, 1958) and to material from off

Mozambique identified by us as B. gilchristi (Sowerby,

1903) [which may or may not be a synonym of

B. bathyraphis]. Bolma millegranosa and B. gilchristi have

smaller adult size, less convex whorls, and a peripheral

cord situated veiy low on the whorl, bearing long

deltoid spines on the periphery, albeit shorter in gilcli risti

than in millegranosa. Bolma millegranosa also differs

by having a flaring outer lip in fully adult specimens.

Two other species which have not been sequenced

resemble Bolma pseudobathijraphis because of their rel-

atively high spire, namely B. girgylla (Reeve, 1843) and

B. kermadecensis Beu and Ponder, 1979. Bolma girgylla

is broadly distributed but rare in the Southwest Pacific

(including New Caledonia); it differs by its flatter base,

primary rows of wide, bilobed spines on the peripheral

and basal cords, and the orange color of the columellar

callus covering only part of the umbilical region. Bolma

kermadecensis, only known from the dead and worn

holotype from the Kermadec Islands, also has a flatter

base, and has a dark pinky fawn color.

Etymology: From its superficial resemblance with

Bolma bathyraphis, with which it had originally been

identified.

Bolma kreipli new species

(Figures 17-20)

Description: Shell small for genus, trochoid, slightly

taller than wide, spire angle 70°, thick and solid.

Teleoconch of 5 3A whorls, first two whorls planispiral,

third whorl with flat sides, last two whorls rather convex

with low peripheral cord bearing strong, projecting

spines (the spines were significantly chipped during

shipping after the photos were taken), basal cord weakly

delimiting convex base. Sculpture of indistinct, fine axial

lamellae and beaded spiral cords, number of cords in-

creasing from 4 on third whorl to 10 above periphery of

last whorl, adapical cord stronger; interspace between

periphery and basal cord with 3 beaded cords; base axi-

ally (radially) lamellate with 6 beaded cords, unevenly

spaced with gap between the 2 cords that surround

umbilical callus and rest of cords. Columella smooth

and evenly rounded, bearing an indistinct tooth

abapically, basal callus veiy thin, transparent, aperture

oval, outer lip barely expanded. No umbilicus. Color

and color pattern variable, background color creamy

white, light brown or beige, with irregular purple, red or

brown flames, base with purple dots irregularly placed

between beads. Columella white, aperture nacreous

within. Operculum thick and heavy, oval with a convex,

wrinkled surface and small, flat marginal edge, white.

Dimensions of holotype: height 14.2 mm, diameter

13.5 mm. Operculum diameter 4.9 mm.

Holotype: MNHN 22827 (lv).

Paratype: 1 (lv), MNHN 22828, from 22°32’S,

167°32/E, 155 m, 9 Sept. 1989 [Smib 5, stn DW82],

Other Material Examined: Musorstom 4: stn

DW203, 22° 36' S, 167°05' E, 105-110 m, 27 Sept. 1985,

2 dd. Lagon: stn 316, 22°35.3/S, 166°54.0' E, 68 m, Nov.

1984, 1 lv; stn 386, 22°37' S, 167°09’ E, 128 m, Nov. 1984,

1 dd; stn 397, 22°39' S, 167° 11' E, 125 m, Nov. 1984, 1 lv.

Type Locality: Between New Caledonia and lie des

Pins, 22°34' S, 167° 10' E, 75 m [Musorstom 4, stn

DW231, I Oct. 1985],

Discussion: We have had no molecular material of

Bolma kreipli, and our comparisons are entirely based

on phenotypic resemblance. Bolma kreipli resembles

B. persica (Dali, 1907) but differs from it by its overall

higher shape, more convex whorls and base, less angular

periphery and basal angle, distinct periumbilical cords,

and non-nacreous columella. At 22 mm, Bolma persica

also reaches a larger adult size than B. kreipli.

Etymology: After Kurt Kreipl, an authority on Bolma

and other turbinids.

Bolma mainbaza new species

(Figures 21-24)

Description: Shell medium-sized for genus, trochoid,

as tall as wide, spire angle about 75°, rather thin shelled.

Teleoconch of 6 whorls, first 2 whorls planispiral, next

whorls regularly convex, separated by narrow, deep

suture; on spire whorls, peripheral cord covered by suc-

cessive whorl, on last whorl not demarcated and re-

sembling any of the spiral cords; basal cord distinctly

Page 96

THE NAUTILUS, Vol. 124, No. 2

Figures 1-16. Bolma species from New Caledonia. 1-7. Bolma castelinae new species. L-3. Holotype, MNI4N 22823, height

25.2 mm. 4. Paratype, MNIIN 22840, adult witli fully developed outer lip, 18°54' S, 163°24' E, 352-397 m [Halical 1, stn DVV02],

height 27,5 mm. 5-6. Juvenile, 24°56' S, 168°22' E, 520 m [Smib 3, stn DW01], height 9.7 mm. 7. Holotype, detail of last whorl. 8-14.

Bolma pseudohathyraphis new species. 8-10. Holotype, MNIIN 22825; height 42 mm. 11-12. Juvenile, 18°56S, 163°24'E, 380-400 m,

Halical 1, stn DW01], height 8,5 mm. 13. Holotype, detail of last whorl. 14. Specimen with unusually spinose sculpture, 24” 45 S,

159° 43' E, 328-463 m [Ebisco, stn CP2505], height 34.6 mm. 15-16. Bolma fuscolineata Alf and Kreipl, 2009, 22°56' S, 167” 15' E,

427-433 m [Norfolk 1, stn DW1733], height 8.6 mm.

A. Alfetal.,2010

Page 97

Figures 17-28. Bolma species. 17-20. Bolma kreipli new species, holotype, MNHN 22827, height 14.2 mm. 21-24. Bolma

mainbaza new species, holotype, MNHN 22829, height 21.2 mm. 25-28. Bolma tantalea new species, holotype, MNHN 22831, height

23.4 mm.

Page 98

THE NAUTILUS, Vol. 124, No. 2

stronger, delimiting poorly defined basal disc. Sculpture

of fine prosocline lamellae and beaded spiral cords,

number above peripheral cord increasing from 2 on

third whorl, to 6 on penultimate whorl and 9 on last

whorl, adapical cord stronger; peripheral cord bearing

spines on spire whorls, simply beaded on last whorl;

interspace between peripheral and basal cords bearing

one beaded cord. Base moderately convex, sculptured by

5 beaded cords, unevenly spaced, with gap to basal cord.

Columella smooth and evenly rounded, with thin,

polished basal callus extending over the base. No umbi-

licus. Outer lip expanded in adult specimens. Back-

ground color light pinkish brown to fawn, beads usually

lighter, white to brown, not forming any pattern. Colu-

mella porcellaneous white. Operculum ovate, outer side

white, regularly convex, weakly pustulose at center.

Dimensions of holotype: Height 21.4 mm, diameter

20.4 mm, operculum largest diameter 8.6 mm. Largest

specimen reaching a size of about 24 mm.

Holotype: MNHN 22829 (lv).

Type locality: Mozambique Channel, off southern

Mozambique, Almirante Leite Bank, 26° 12' S, 35°02' E,

228-230 m [Mainbaza, stn DW3167, 16 April 2009].

Paratypes: 14: MNHN 22830, I 1 (6 lv, 5 dd); Natal

Museum L7886/T2579, 1 (lv); Museu de Historia Natu-

ral de Maputo, Mozambique, 1 (dd); Coll. J. Rosado,

Maputo, 1 (lv); all from the type locality.

Remarks: Magalie Castelin has obtained DNA from

the tissues of this new species, but sequencing has, at the

time of writing, been unsuccessful. Our comparison with

other species is thus purely phenotypical. Of the six spe-

cies of Bolma recorded until now from the southwestern

Indian Ocean, Bolma mainbaza resembles B. flava Beu

and Ponder, 1979 [a full species, or a geographical sub-

species of B. tamikoana (Shikama, 1973), as treated by

Beu and Ponder] but the latter differs by having more

depressed whorls, a distinct, spine-bearing peripheral

cord, more numerous and finer spiral cords (10 above

periphery of last whorl, 3 between peripheral and basal

cords, 16 on base), and a color pattern consisting of

brownish to purplish flames on a yellowish background;

B. mainbaza lacks spines and is fawn-colored with irreg-

ularly scattered, small, well defined brown spots.

Etymology: Named after the cruise Mainbaza, an

acronym for MAputo, /Miambane, BAzaruto and

ZAmbeze, Mozambique localities off of which deep-

water transects were carried out.

Bolma tantalea new species

(Figures 25-28)

Description: Shell of average size for the genus, tro-

choid, slightly broader than tall (h/d — 0.95), spire angle

about 85°, shell thick and solid. Teleoconch of about

5.5 whorls, suture shallow, adapical whorls almost flat,

last whorl moderately convex, periphery and basal disc

poorly demarcated. First 2.5 teleoconconeh whorls

smooth between subsutural, strongly beaded cord and

peripheral cord bearing blunt spines, 14 per whorl, cov-

ered by successive whorl. Subadult and adult whorls with

narrow smooth ramp adapically of subsutural cord, addi-

tional spiral beaded cords occupying space between

subsutural and spineless, peripheral cord; 4 cords on 3rd

whorl, 5 on exposed part of penultimate whorl, 7 plus a

couple of secondary ones above periphery of on last

whorl; 2 primary and 2 secondary cords between periph-

ery and basal angle, beads on periphery and basal cord

coalescent. Base slightly convex, sculptured with 2 weakly

beaded and ea. 12 smooth spiral cords that become'

obsolete toward columellar region. Columella smooth

and evenly rounded, umbilicus closed by thick, slightly

yellowish white polished callus, covering about 1/3 of

the basal disc. Outer lip hardly reflected at all. Back-

ground color pinkish ivory, with darker, 1 irownish-purple

axial veins. Columella and aperture nacreous. Opercu-

lum rounded, outer side white, nucleus veiy slightly

depressed, greenish brown. Dimension of holotype:

Height 23.4mm, diameter 26.3nnn, operculum largest

diameter 10.0 mm.

Holotype: MNHN 22831 (lv).

Paratype: MNHN 22832, 1 (dd) from off Raiatea,

Society Islands, 16°53' S, 151°2T W, 440-490 m, 18

Oct. 2009 [Tarasoc, stn DW3451],

Material Examined and Distribution: Only known

from the type material and several fragments from the

western part of the Tuamotus chain attributed to the

species.

Type Locality: French Polynesia, Society Islands,

Tahiti, 17°48' S, 149°22' W, 390-790 m [Tarasoc, stn

DW3488, 23 Oct. 2009],

Remarks: Bolma tantalea is veiy distinctive among

South Pacific Bolmas by its veiy compact overall appear-

ance. It vaguely resembles B. recens which differs by a

pointed spire, deep and often even canaliculate suture,

well marked peripheral and basal angles separated by an

almost flat interspace, a spiral sculpture with fewer (usu-

ally up to 5 above periphery) beaded cords and short

triangular spines on the periphery, at least on spire

whorls. Spineless forms of Bolma tamikoana can be sep-

arated by their orange columellar callus. Bolma opaoana

has a pointed spire and its color is fawn with brownish

flames, and a slight orange blotch on the columella and

columellar callus. Bolma midwaijensis Habe and Kosuge,

1970, has a pointed spire and deep suture, and its color is

whitish with pink clouds.

Etymology: Tantaleus, - a , -um, is an adjective formed

after Tantalus, the mythological character symbolic of

torment. During the Tarasoc cruise only tantalizing shell

fragments were first sampled, then during the third week

a broken adult was taken, and the live-taken holotype

was finally obtained after more than 120 dredge hauls,

just three days before the end of the cruise.

A. All et al., 2010

Page 99

ACKNOWLEDGMENTS

The New Caledonia material originates From many

cruises listed by Bouchet et al. (2008), and we are

especially grateful to our colleagues Marie-Catherine

Boisselier, Magalie Caste lin, Pierre Lozouet, Bertrand

Richer de Forges, and Sarah Samadi for companionship

at sea and unpublished molecular results in the

laboratory. The specimens from off Mozambique were

collected by R.V. Vizconde de Eza during the MAIN-

BAZA cruise in April 2009. The cruise was operated by

Museum National d’Histoire Naturelle (MNHN) and

Institute Espahol de Oceanografia (IOE), as part of a

cluster of Mozambique-Madagascar expeditions funded

by the Total Foundation, Prince Albert II ol Monaco

Foundation, and Stavros Niarchos Foundation, and

conducted by VI N 1 1 N and Pro-Natura International

(PNI). Philippe Bouchet is grateful to Ana Ramos and

Eduardo Balguerias for making this cruise possible.

Like many other expeditions in the Tropical Deep-Sea

Benthos program, the Tarasoc cruise took place on

board IRD’s (Institnt de Recherche pour le Developpe-

ment) R.V. Alis, and its success owes much to the skills

ol its officers, Raymond Proner, |ean-Franyois Barazer

and Loi'c Le Gofl. Finally, we are grateful to Magalie

Castelin tor having made her molecular results available

to us to facilitate species-level comparisons ol the new

species described in this paper.

LITERATURE CITED

All, A. and K. Kreipl. 2009. An updated list of the recent Bolma

species (Gastropoda: Turbinidae) with description of two

new species from French Polynesia and New Caledonia.

Novapex 10: 17-24.

Beu, A. and W. Ponder. 1979. A revision of the species of

Bolma Risso, 1826 (Gastropoda: Turbinidae). Records of

the Australian Museum 32: 1-68.

Bouchet, P. and B. Metivier. 1983. The genus Bolma (Mollusca:

Gastropoda) in the bathyal zone of New Caledonia, with

description of a new species. Venus 42: 8-12.

Bouchet, P., V. Heros, P. Lozouet, and P. Maestrati. 2008.

A quarter-century ol deep-sea malacologieal exploration in

the South and West Pacific: Where do we stand? How far to

go? Tropical Deep Sea Benthos, volume 25. Memoires du

Museum National d’Histoire Naturelle 196: 9-40.

Meyer, C.P, J.B. Geller, and G. Paulay. 2005. Fine scale

endemism on coral reefs: archipelagic differentiation in

turbinid gastropods. Evolution 59: 113-125.

THE NAUTILUS 124(2): 100-106, 2010

Page 100

The use of aquatic plants by populations of the zebra mussel

( Dreissena polymorpha) (Bivalvia: Dreissenidae) in a small

glacial lake

B.L. Bodamer1

M.L. Ostrofsky2

Biolog)' Department

Allegheny College

Meadville, PA 16335

ABSTRACT

We examined the early life history of the zebra mussel

(. Dreissena polymorpha) in a small Pennsylvania lake with lim-

ited natural hard substrate. Veligers first appear in May, and

settled on Nuphar (Yellow Water Lily) stems and concrete sub-

strates in equal densities. Later cohorts, however, did not settle

on the stems. Juveniles on stems abruptly abandoned their

attachment in late August as the plant tissue began senescence.

Aquarium experiments demonstrated that juveniles retained the

ability to seek and find alternate substrates even after several

months. Year-old zebra mussels were markedly unsuccessful in

comparison. We speculate that in lakes with limited natural hard

substrates aquatic plants may play an important role in zebra

mussel recruitment, although juveniles must be able to locate

alternate substrates as plant populations senesce at the end

of the season. The resulting high mortality may limit mussel

populations in these lakes.

Additional keywords: Invasions, substrate, life history, aquatic

macrophytes

INTRODUCTION

Following the introduction of the zebra mussel ( Dreissena

polymorpha) to Lake St. Clair in the 1980s, much atten-

tion has been focused on the rapid dispersal and the

environmental requirements of this invader (Griffiths

et al. 1991, Strayer 1991, Hincks and Mackie 1997).

Ludyanskiy et al. (1993) predicted that by the year 2000

the zebra mussel would inhabit all of North America’s

rivers, lakes, and reservoirs that fit within its broad range

of ecological requirements. However, due to the limita-

tions of overland dispersal the invasion of small inland

lakes disconnected from navigable waters is taking much

longer than initially anticipated (Kraft and Johnson 2000,

1 Current address: The Lake Erie Center, University of Toledo,

6200 Bayshore Rd, Oregon, OH 43618 USA

“ Corresponding author: [email protected]

Bossenbroek et al. 2001). The glaciated portion of north-

western Pennsylvania, for example, has eight natural

lakes all between 18 and 74 km from the south shore of

Lake Erie, the most immediate source of veligers and

adults, and all meeting the ecological requirements of

D. polymorpha. To date, however, only two of them have

established populations of D. polymorpha (Butkas and

Ostrofsky, 2006) in spite of considerable recreational boat

traffic among these inland lakes, and between these lakes

and Lake Erie where D. polymorpha was first observed

in 1989 (Griffiths et al. 1991). Observations from other

inland lake districts in Illinois, Indiana, Michigan,

New York, and Wisconsin have reported similarly slow

dispersal and colonization (Miller and Haynes 1997, Kraft

and Johnson 2000, Johnson et al. 2001). Consequently,

the bulk of the published North American work on

D. polymorpha has been from the Great Lakes and major

river systems. The effects of this invader on small, inland

lake ecosystems have received far less attention.

One of the characteristics of lakes in northwestern

Pennsylvania and lakes in similar geographical settings

is the relative paucity of natural hard substrates. These

lakes tend to be small, with limited wind-generated wave

energy to move fine sediments offshore. This combina-

tion of characters results in lakes with soft, muddy or

peaty sediments right up to a shoreline that transitions

through a zone of floating-leaved and emergent aquatic

vascular plants. Rock outcrops and gravel bars are excep-

tionally rare. With the exception of the shells of native

unionid mussels, the hard substrates that do exist are

invariably man-made: docks, pilings, retaining walls, boat

hulls, and waterlogged pieces of wood and other debris.

Several studies have suggested that the colonization suc-

cess and ultimate carrying capacity of D. polymorpha

populations is determined by the availability of suitable

hard substrates for attachment rather than by the quality

and quantity of filterable food resources (Brady et al.

1995, Grigorovich and Babko 1997, Lewandowski 2001,

Burlakova et al. 2006). There have been several studies

that investigate the relative preferences displayed lor

B.L. Bodamer and M.L. Ostrofsky, 2010

Page 101

substrate type, orientation, and texture by settling

D. polymorpha veligers (Marsden and Lansky 2000,

Kobak 2004, Czarnolyski, et al. 2004) but one possible

substrate that has not received much attention is the

surface of aquatic vascular plants (Lewandowski 2001).

Dreissena polymorpha is known to attach to aquatic

vascular plants (Horvath and Lamberti 1997, Diggins

et al. 2004, Musko and Bako 2005). Hence, vascular

plants may play an important role in the establishment

and persistence of invasive populations in lakes with lim-

ited alternate hard substrates. However, while aquatic

vascular plants offer considerable surface area, and often

grow in dense stands that confer attached mussels some

protection from predation by fish, they are seasonal and

lack long term stability (Grigorovich and Babko 1997,

Ozimek 1997). Most species rapidly senesee with the

onset of cooler weather and shorter day lengths. To

survive, attached biota must have the ability to abandon

senescent plants and seek another, more permanent

substrate.

In order to fully understand the ecology of the zebra

mussel and the impacts it will cause as it continues to

spread throughout North America, it is essential that we

understand species interactions within small-lake ecosys-

tems. In this study, we examined the early life history of a

zebra mussel population in a small inland lake in Pennsyl-

vania. We were particularly interested in the potential role

of aquatic vegetation in a lake that otherwise provides lew

hard substrates. We sought to determine if aquatic plants

could provide a substrate that was as acceptable to settling

D. polymorpha veligers as more traditional hard sub-

strates, and if, at the end of the vegetative growing season,

settled juveniles retained the capacity to seek alternate

substrates as the plant tissue senesced.

MATERIALS AND METHODS

All fieldwork was conducted in Sandy Lake, a small

(~ 60 ha), moderately hard (total alkalinity ~ 70 mg/L)

kettle lake located in Mercer County, Pennsylvania (41°

20.7 L N, 80°06.43’ W). Sandy Lake has a drainage basin

area of only 7.2 km" consisting mostly of forest (52.6%)

and low intensity agriculture (pasture/hay 39.7%, row

crops 3.6%; USGS, 2000). Although no bathymetric

map has been made to date, the maximum noted depth

was 12 m. The lake stratifies from May through mid-

October, with the thermocline at approximately 5 m.

Hypolimnetie water below 9 m became anoxic by

early July. Springtime total phosphorus concentration

(~ 13 ug/L) and summer average Secchi disk visibility

(3.5 m) suggest that the lake is oligo-mesotrophic

(Ostrofsky, unpubl.). Sandy Lake is used primarily for

fishing, swimming, and waterskiing. Dreissena polymorpha

were first observed in the lake in 2000 (J. Widel, Lakeside

Park Co., personal communication) and have been a con-

spicuous feature on hard surfaces ever since.

Water samples for the enumeration of planktonic veli-

gers were collected weekly from three mid-lake locations

from mid-May to late-October 2004 (Figure 1). Two

liters of epilimnetic water from each location were fil-

tered through 0.45 pm membrane filters. Filters were

dried, cleared with immersion oil, and mounted on

slides. Veligers were identified using cross-polarized

microscopy (Johnson 1995). Lengths of 200 (or n, if

n< 200) veligers were measured to the nearest 10 pm

using an ocular micrometer.

We monitored settlement of juvenile D. polymorpha

on both artificial substrates and aquatic vascular plant

surfaces. We used 0.093 m2 concrete tiles (12"xl2")

placed in three lake locations (Figure 1) at a depth of

approximately 1.5 meters. Tiles were put in the lake in

May and retrieved in late August/September after veli-

gers had disappeared from the water column. Juveniles

found were preserved in 70% ethanol. The length of

each juvenile was measured to the nearest 0.1 mm using

a dissecting microscope and an ocular micrometer. We

monitored the settlement of juvenile D. polymorpha on

the submersed stems of the Yellow Water Lily Nuphar

variegata. We collected ten individual stems (~0.75 m in

length) from each of live macrophyte beds around the

lake at weekly intervals from mid-May through Septem-

ber. Each stem was scraped to remove all attached

organisms. All scrapings were preserved in 70% ethanol

until examined. The total number of juveniles found on

each stem was recorded. For each date sampled 200 (or

n, if n< 200) juveniles were randomly selected and mea-

sured to the nearest 0.1 mm. Both veligers and settled

juveniles were grouped into size classes and size-

frequency graphs were constructed to estimate spawning

and settling cohorts across the growing season.

To determine the ability of D polt/moipha to migrate

to alternate substrates we suspended lake-collected mac-

rophyte stems with 100 attached juvenile mussels in

coarse mesh netting at the surface of each of 3 replicate

37 L (10 gal.) aquaria in the lab. The bottom of each

aquarium was covered with a patchwork of unglazed

ceramic tiles (15x15 cm) and fine lake sediments in a

LI substrate/sediment ratio. Each tank was filled with

aerated lake water. After two weeks the macrophyte

Figure 1. Map of Sandy Lake, Pennsylvania showing sam-

pling locations for Dreissena polymorpha veligers, Nuphar

beds, and artificial substrates.

Page 102

THE NAUTILUS, Vol. 124, No. 2

stems had seneseed, and stems, tiles, and sediments

were examined for juveniles. We used to test the null

hypothesis of random settling (frequencies on tiles =

frequencies on soft sediment).

To examine differences in the ability to seek and find

new substrate as a function of mussel age, we established

8 replicate 37 L aquaria in the lab, each with fine lake

sediment, aerated lake water, and a single tile giving a 1:5

tile to soft sediment ratio. To each aquarium we intro-

duced 5 juvenile (6-1 1mm) and 5 adult (20-30 mm)

D. polymorpha individuals to the soft sediment. Very

few lake-collected mussels were found between 11 and

20 mm suggesting that these two size classes were from

different spawning seasons. Tiles were examined daily

and the number of juveniles and adults eensused for

1 week. The rates at which juvenile vs. adult mussels

accumulated on the tiles was taken as a measure of their

ability to find alternate substrates.

RESULTS

Veligers were first observed in the plankton in late May

when the epilimnetic water temperature was 21°C.

There were no significant differences (p > 0.05, ANOVA)

in veliger densities among the three lake sampling sites so

data from all sites were pooled. Veliger density increased

rapidly to a maximum of 17,500/m3 (± 5,635 s.e.) in late

June, then rapidly decreased, disappearing from the

plankton by early August (Figure 2). Measured veligers

varied in length from 60 to 250 pm, and size-frequency

analysis (Figure 3) and changes in density suggest the

presence of three cohorts: large ones in late May and late

June, and a veiy much smaller one in late July.

Settled larvae first appeared on Nuphar stems in late

June (Figure 4), reaching maximum densities in mid-July

of 62 (±20.7 s.e.) individuals per stem (approximately

1 individual/cm"). Settled juveniles showed a strong ten-

dency to aggregate on a few stems rather than to accu-

mulate evenly among all available stems. In 50% of the

25000 a

20000 -

O h- CO O CO CO T- CD CNJ

CM CNJOCNJ COOt-CNCNI O x-

lo lo co cooo

Date

Figure 2. Mean Dreisseua polymorpha veliger densities (± 1

std. error) in the epilimnion of Sandy Lake.

site x date collections the varianceunean ratio of settled

juveniles on stems was significantly greater than one

(yy-test). The smallest measured juveniles were 200 pm,

approximately the same as the maximum veliger size in

A B C D E

Size Class

Figure 3. Size-frequency distribution of Sandy Lake Dreissena

polymorpha veligers. Lines separate different cohorts suggested

by both density and size distribution data. Size class A = <110 p,

B = 111-150 p, C = 151-190 p, D = 191-230 p, E = >231 p.

B.L. Bodamer and M.L. Ostrofsky, 2010

Page 103

Figure 4. Mean density of juvenile Dreissena polymorpha

(± 1 std. error) on stems of Nuphar variegata in Sandy Lake.

the plankton. Visual analysis of size-frequency data of

the settled juveniles on stems (Figure 5) suggested

only a single cohort with high initial mortality (77%)

but very little mortality after late July. Juveniles

abruptly disappeared from stems after late August. Adult

D. polymorpha between 6 and 17 mm in length were

occasionally observed attached to Nuphar stems, partic-

ularly early in the season. Individuals of this size were

undoubtedly from the previous growing season. Con-

crete tiles collected at the end of the summer had densi-

ties of settled juveniles ranging from 0.11 to 2.69

individuals per cm" (mean =1.0, s.e. = 0.9). There was

no significant difference between the density of settled

juveniles on concrete tiles and the maximum density

measured on Nuphar stems (p > 0.05, t-test).

In the laboratory experiments approximately half

(46%) of the juveniles on suspended vascular plant stems

in the aquaria abandoned their attachment sites within

two weeks as the stem senesced (Table 1). We antici-

pated equal numbers would be recovered from the tiles

and from soft sediments if displaced juveniles were inca-

pable of migrating to firm substrates. We found that all

of the displaced juveniles were recovered either on the

tiles (26.7T7.7 s.e.) or attached to the aquarium walls

(19.0T5.1 s.e.). None was recovered from the soft sedi-

ment. Those that remained attached to the plant mate-

rial were assumed to be dead.

In the migration experiment comparing juveniles

and adults, juveniles were found on the tile early and their

numbers steadily increased (Figure 6). Adults appeared

on the tiles late and in veiy small numbers. Bates of arrival

on the hard substrate were 3.54 and 0.29 individuals/day

for juveniles and adults, respectively. These rates were

significantly different (p < 0.05, t-test lor slopes).

DISCUSSION

An overview of the life history of Dreissena polymorpha

given by Ludyanskiy et al. (1993) based largely on the

A B C D E F G

Size Class

Figure 5. Size-frequency distribution of juveniles on Nuphar

variegata stems. Data suggest a single cohort. Size class

A = <400 p, B = 401-900 p, C = 901-1400 g, D = 1401

1900 g. E = 1901-2400 p. F = 2401-2900 p, G = >2901 p.

European literature suggests that initial veliger size is

about 70 pm and that these veligers increase rapidly in

size (up to 300 pm) in 5 days to 5 weeks, at which time

they can no longer remain suspended in the plankton and

Page 104

THE NAUTILUS, Vol. 124, No. 2

Table 1. Distribution of juvenile mussels initially attached to

senescing aquatic plants after two weeks. Approximately 46%

of the mussels left the plants and successfully located an

alternate hard substrate for reattachment. No mussels were

found in the soft sediment.

Figure 6. Migration of juvenile and adult Dreissena

pohjmorpha from soft sediment to hard tile substrate in aquarium

experiment.

settle on hard substrates. Veligers first appeared in Sandy

Lake on May 20, and rapidly increased to a maximum

density of about 1 7,500/m3. The smallest veligers were

60 pm, and the largest were 250 pm. We tentatively iden-

tified three cohorts based on size-frequency analysis.

The first juveniles appeared on Nuphar stems on

June 30, and by July 21 had reached a mean density of

62 individuals/stem (approximately 1 individual/cm3).

Size-frequency analysis of settled juveniles suggested

only a single cohort (in contrast to possibly three veliger

cohorts). Similarly, Wainman et al. (1996) found only a

single three-week recruitment (settling) period in Lake

Erie, also in July. We are confident that the first veliger

cohort was the source of the settled juveniles because

the smallest settled juveniles were approximately the

same size as the largest of the veligers, and they

overlapped temporally. The single cohort that success-

fully settled on Nuphar stems appeared to suffer high

initial mortality, falling from a density of 62 individuals/

stem to 1 1/stem in the first week. There was no further

significant decrease in density until September 3, when

densities fell to zero.

The abrupt loss of juveniles from plant stems at the

end of August could be a consequence of increased

predation — those on plant stems perhaps being particu-

larly vulnerable/visible/available — or could be the result

of a mass abandonment of these attachment sites as a

consequence of some perceived change in substrate

quality. In late summer, Nuphar stems become heavily

coated with epiphytic microorganisms, and the stems

lose their firmness - either condition might signal a dete-

rioration of substrate quality to the mussels. That

Nuphar stems are attractive settlement sites early in the

summer is supported by our observation that mean juve-

nile density on stems is no different from mean density

on concrete artificial substrates collected at the end of

the summer although the aggregated distribution on

plant stems, and the data from the literature on other

hard surfaces suggest that they are attracted by slight

differences among otherwise similar surfaces or to each

other (Wainman, et al. 1996). The lack of any evidence

for the settlement of the second and third veliger cohorts

on stems as the season progresses suggests that these

sites become less attractive.

The fate of juveniles that abandon their attachment to

Nuphar stems is unknown. Newly settled juveniles have

the ability to seek alternate attachment sites by crawling

or by using byssal threads to resuspend themselves in the

water column and resettle elsewhere (Griffiths, et al.

1991, Marsden and Lansky 2000), and Martel (1993)

has documented juveniles up to 2 mm in length in the

plankton of Lake Erie under conditions of high waves

and strong currents. Lewandowski (1982) has noted the

presence of plant remains in the byssus of 1 and 2 year

old individuals found in benthic colonies. We are aware

of no studies that have directly observed the fate of

established juveniles that have abandoned their attach-

ment sites after several weeks, however. Juveniles leaving

attachment sites at the end of the summer in Sandy Lake

were large enough (77% were greater than 2 mm in

length) that resuspension is an unlikely option. Juveniles

may simply fall to the sediment surface and crawl seek-

ing a better substrate.

The aquarium experiments did show that these large

juveniles were capable of locating and successfully

attaching to hard substrates after leaving senescing plant

material. All of those that abandoned the plant stems in

aquaria were found either on the tiles or on the aquar-

ium walls. None was found on the soft sediments. This

ability to find alternate substrates is lost with time,

and year-old individuals were markedly unsuccessful

compared to the younger cohort. At Sandy Lake we

frequently encountered relatively large (6-17 mm)

D. polymorpha individuals attached to plant stems or to

the undersides of Nuphar leaves, particularly early in the

season. We speculate that these individuals represent the

previous year’s cohort that abandoned plant stems, failed

to find an alternate substrate, persisted on the surface of

the plant litter in the littoral zone over the winter, then

had a serendipitous encounter with an emerging Nuphar

shoot the following spring. Lewandowski (1982) has also

noted that 99.5% of the individuals found on plants are

less than 0.5 mm in length, indicating that they belong to

the youngest cohorts.

B.L. Bodamer and M.L. Ostrofsky, 2010

Page 105

In Sandy Lake, and in other inland lakes with limited

natural hard substrates it is likely that a significant por-

tion of the annual D. polymorpha settlement occurs on

plant surfaces - not only the relatively firm stems of

Nuphar and emergent vegetation, but on the softer foliage

of submersed plants as well. The available surface area

provided by plants vastly exceeds that of alternate attach-

ment sites. While the density of juvenile mussels on plants

may be comparable to that on other substrates, mortality

is considerably higher as a result of the need to abandon

the plant surfaces with plant senescence, and the low

probability of encountering an alternate site even though

juveniles retain the ability to seek these sites. The

resulting high mortality may be sufficient to limit the

size of the adult population in lakes with limited hard

substrate.

Why have zebra mussels failed to colonize small inland

lakes in the midwestern U S as anticipated by Ludyanskiy

et al. (1993)? Johnson et al. (2001), noting low coloniza-

tion success in spite of dispersal events estimated in the

hundreds or thousands, cite three possible reasons for

this failure. First overland transport is inefficient and

many mussels attached to boats or to aquatic plants

entangled in boats and trailers, or carried in bait wells

or in bilge water fall off or die before reaching a new

colonization site. Second, boaters do not visit lakes ran-

domly, but rather visit a small subset of the most popular

ones and long-distance dispersal fits a gravity model

rather than a diffusion model (Bossenbroek, et al. 2001).

Finally, overland transport and inoculation of new sites

may occasionally be successful, but the colonists fail to

found new populations. The causes of this failure are

certainly varied. Butkas and Ostrofsky (2006) reported

evidence of a failed introduction in Canadohta Lake

likely due to too small an inoculum. Other introductions

may fail as a result of inhospitable chemical or physical

characteristics of the new site, including a paucity of

favorable substrates for attachment. Lewandowski

(2001) has estimated the survival of settling veligers to

be usually less than 1%, and even in lakes with unusually

well developed littoral zones less than 5% simply by

failing to find an appropriate substrate. Further, those

that do find substrates may not survive winter freezing

or ice scour (Brady et al. 1995) if those substrates are in

shallow water.

Our data suggest that the earliest cohort of settling

veligers in Sandy Lake do not discriminate among sub-

strates in that there was no significant difference

between the density of juveniles on artificial hard sub-

strates (concrete tiles) and their density on Nuphar

stems. Karatayev et al. (1998) observed similar results in

a number of European lakes when comparing juvenile

mussel densities on a number of natural substrates

including aquatic plants. Later cohorts in Sandy Lake

did not settle on the stems, or settled on them in very

much reduced numbers, evidently finding them less suit-

able than did the earlier cohort. Nevertheless, the sur-

face area of plant tissue available for settlement greatly

exceeds the area of other substrates (Brady et al. 1995,

Ozimek 1997), and Lewandowski (1982) estimated that

more than 85% of the mussel population in 26 Masurian

(Poland) lakes were using aquatic plants as substrates.

However, the growing season of aquatic plants is shorter

than the life of mussels, and on senescence mussels must

abandon plant surfaces and seek alternate substrates if

they are to survive. In Sandy Lake the density of juve-

niles on plants declined abruptly at the end of August.

Lewandowski (2001) similarly found that populations of

first year mussels on plants decreased by 78% between

August and September in Lake Czos due to plant senes-

cence. Larger declines were seen in older mussels. Our

laboratory experiments illustrate that these first year dis-

placed mussels have the ability to migrate in search of

alternate substrates, and our finding larger, second year

old mussels occasionally on plant surfaces indicates that

at least some are successful in that search. Lewandowski

(1983) reported similar findings — that 2 to 3 year old

mussels were found on plant surfaces in low numbers,

99.8% of the individuals were juveniles that had settled

that year. However the cumulative effect of low settle-

ment success and low survival of those settling on aquatic

plants must severely limit the populations of zebra mus-

sels in lakes lacking more permanent hard substrates.

ACKNOWLEDGMENTS

We are grateful to | . Widel for access to Sandy Lake and

to j. Cass for his capable field assistance.

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THE NAUTILUS 124(2): 107-111, 2010

Page 107

Description of Calliotropis ceciliae new species (Gastropoda:

Chilodontidae: Calliotropinae) from off Chile

Claude Vilvens

Scientific collaborator to the Museum national d’Histoire

naturelle, Paris.

Rue de Hermalle, 113

B-46S0 Oupeye

BELGIUM

[email protected]

Javier Sellanes

Universidad Catoliea del Norte, Facultad de Ciencias del M ar

Larrondo 1281 Coquimbo, CHILE

and

Centro de Investigaeion Oceanografica en el Pacffico Sur-oriental

(COPAS)

Universidad de Concepcion

Concepcion, CHILE

[email protected]