THE NAUTILUS

QL

HOI

N3M

£2

Volume 131, Number 1

March 28, 2017

ISSN 0028-1344

A quarterly devoted

to malacology .

EDITOR-IN-CHIEF

Jose H. Leal

The Bailey- Matthews National

Shell Museum

3075 Sanibel-Captiva Road

Sanibel, FL 33957 USA

EDITOR EMERITUS

M. G. Harasewyeh

Department of Invertebrate Zoology

National Museum of

Natural History

Smithsonian Institution

Washington, DC 20560 USA

CONSULTING EDITORS

Riidiger Bieler

Department of Invertebrates

Field Museum of

Natural History

Chicago, IL 60605 USA

Arthur E. Bogan

North Carolina State Museum of

Natural Sciences

Raleigh, NC 27626 USA

Philippe Bouchet

Laboratoire de Biologie des

Invertebres Marins et Malacologie

Museum National d’Histoire Naturelle

55, rue Buffon

Paris, 75005 FRANCE

Robert IT Cowie

Center for Conservation Research

and Training

University of Hawaii

3050 Maile Way, Gilmore 409

Honolulu, HI 96822 USA

Kenneth A. Hayes

Department of Biology

Howard University

Washington, DC 20001 USA

Steffen Kiel

Department of Paleobiology

Swedish Museum of Natural History

Box 50007

104 05 Stockholm, SWEDEN

Harry G. Lee

4132 Ortega Forest Drive

Jacksonville, FL 32210 USA

Charles Lydeard

Biodiversity and Systematics

Department of Biological Sciences

University of Alabama

Tuscaloosa, AL 35487 USA

Bruce A. Marshall

Museum of New Zealand

Te Papa Tongarewa

P.O. Box 467

Wellington, NEW ZEALAND

Paula M. Mikkelsen

Paleontological Research

Institution

1259 Trumansburg Road

Ithaca, NY 14850 USA

Diarmaid O Foighil

Museum of Zoology and Department

of Biology

University of Michigan

Ann Arbor, MI 48109-1079 USA

Gustav Paulay

Florida Museum of Natural History

University of Florida

Gainesville, FL 32611-2035 USA

Gary Rosenberg

Department of Mollusks

The Academy of Natural Sciences

1900 Benjamin Franklin Parkway

Philadelphia, PA 19103 USA

Elizabeth Shea

Mollusk Department

Delaware Museum of

Natural History

Wilmington, DE 19807 USA

Angel Valdes

Department of Malacology

Natural History Museum

of Los Angeles County

900 Exposition Boulevard

Los Angeles, CA 90007 USA

Geerat |. Vermeij

Department of Geology

University of California at Davis

Davis, CA 95616 USA

G. Thomas Watters

Aquatic Ecology Laboratory

1314 Kinnear Road

Columbus, OH 43212-1194 USA

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THE^NAUTILU S

Volume 131, Number 1

March 28, 2017

ISSN 0028-1344

CONTENTS

Mollusks in Peril 2016 Forum Section

Robert H. Cowie Measuring the Sixth Extinction: What do mollusks tell us? . 3

Claire Regnier

Renoit Fontaine

Philippe Bouehet

Julia D. Sigwart Is mining the seabed bad lor mollusks? . 43

Chong Chen

Leigh Marsh

Regular Articles

Yusuke Miyajima Taxonomic reexamination of three vesicomyid species (Bivalvia) from the

Takami Nobuhara middle Miocene Bessho Formation in Nagano Prefecture, central Japan,

Hakuiehi Koike with notes on vesicomyid diversity . 51

Kathryn E. Perez A new species of South Texas scrubsnail, Praticolella (von Martens, 1892)

Eli Ruiz (Gastropoda: Polygyridae) . 67

Mareo Martinez Cruz

Russell L. Minton

Shuqian Zhang A new genus and species of Neomphalidae from a hydrothermal vent ol the

Suping Zhang Manus Back-Arc Basin, western Pacific (Gastropoda: Neomphalina) . 76

Laura Regina Alvarez-Cerrillo A remarkable infestation of epibionts and endobionts of an edible chiton

Paul Valentich-Scott (Polyplacophora: Chitonidae) from the Mexican tropical Pacific . 87

William A. Newman

Angel Valdes A new species of Parvaplustrum Powell, 1951 (Gastropoda: Heterobranchia:

Terrence M. Gosliner Aplustridae) from the northeastern Pacific . 97

Anders Waren

Book Review . 101

Notices . 103

f m 0 4 2017 J

mollusks in peril

2016 forum

presented by

^ BAILEY-MATTHEWS

^ NATIONAL SHELL MUSEUM

The first two articles in this issue derive from the presentations given at the Mollusks in Peril 2016

Forum. The Forum took place at the Bailey-Matthews National Shell Museum on May 22-24, 2016, and

encompassed hour-long presentations by eleven specialists in conservation, systematics, and ecology of

mollusks. The subjects spanned a broad range of subjects that included Pacific island land snail

conservation, threats to pelagic mollusks, freshwater mollusks in peril, and ocean acidification impacts on

larval growth. The two papers presented here cover an update to recent global estimates of extinct and

endangered mollusks (Cowie, Regnier, Fontaine, and Bouchet) and an assessment of the impacts of

mining on deep-sea mollusks (Sigwart, Chen, and Marsh). I want to thank Shell Museum Executive

Director and Forum co-organizer Dorrie Hipschman and major sponsors Smoky and Stephanie Payson for

their enthusiasm and hard work. Mollusks in Peril will continue with a special session to be held at the

upcoming meeting of the American Malacological Society (July 16-21, 2017), at the University of

Delaware (http://www.delmnh.org/ams20 1 7).

Jose H. Leal, Ph.D.

Science Director and Curator

Bailey-Matthews National Shell Museum

Editor, The Nautilus

THE NAUTILUS 131(1):3-41, 2017

Page 3

Measuring the Sixth Extinction: what do mollusks tell us?

Robert H. Cowie

Pacific Biosciences Research Center

University ol Hawaii

Honolulu, HI 96822 USA

[email protected]

Claire Regnier

Renoit Fontaine

Philippe Bouchet

Museum national d’Histoire naturelle

Paris 75005, FRANCE

ABSTRACT

The Internationa] Union for Conservation ol Nature (IUCN) is

the premier global biodiversity conservation organization. Its

Red List is a rigorous vehicle for assessing the conservation

status of plant and animal species. However, although all ani¬

mal and bird species recognized by IUCN have been evalu¬

ated, only a tiny fraction of invertebrates have been evaluated.

As a measure of the numbers of extinct species (since around

the year 1500) the Red List is probably quite accurate for birds

and mammals, but severely underestimates the numbers for

invertebrates. Nonetheless, molluscs stand out as the major

group most severely impacted by extinction, with 297 of the

744 animal species listed as extinct in the third issue of the

2016 Red List. Here we review efforts to obtain a more realis¬

tic, albeit less rigorous, assessment of the numbers of extinct

mollusk species. Our approach has been based on biblio¬

graphic research and consultation with experts, rather than

following die highly detailed but restrictive IUCN Categories

and Criteria. In 2009, this led to an assessment that 533 mol¬

lusk species were extinct, far more than the number on the

Red List. In the present study we revisited this approach and

here list 638 species as extinct, 380 as possibly extinct, and

14 as extinct in the wild, a total of 1,032 species in these

combined categories, and more than twice as many as listed by

IUCN in these categories. However, this approach only con¬

siders species for which information is available; it is therefore

biased. In a study published in 2015 we developed an alterna¬

tive approach, based on a random global sample of land snails,

and estimated that 3,000-5,100 mollusk species have gone

extinct. We review the main reasons for these extinctions: hab¬

itat destruction, impacts of introduced species, exploitation and

collecting, and, potentially, climate change, and discuss rele¬

vant case studies. Oceanic island land snails, especially those of

Pacific islands, have suffered the greatest proportion of the

extinctions, with some species having gone extinct before being

discovered and described scientifically. The Amastridae, an

endemic Hawaiian family of 325 recognized species, may have

lost all but 18 species. We outline the phases in this catastro¬

phe: 1) pre-human and/or prehistoric extinction, either natural

or anthropogenic, with species known only as fossils/subfossils;

2) extinction due to habitat destruction and introduction of a

number of alien species by Pacific island people as they settled

the islands; 3) extinction due to extensive habitat destruction

and introduction of highly destructive invasive alien species

following colonization by Westerners; 4) extinction following

the advent of large-scale agriculture at the end of the 19th

Century, at the time of a major increase in the land snail

extinction rate globally; 5) extinction due to increased military

activity, tourism, commerce, urbanization and the concomittant

rapidly increasing introduction of invasive species after the

Second World War. Extrapolating from our assessments of

mollusks, we estimate that approximately 7.5-13% of all spe¬

cies have gone extinct since around year 1500. This is orders of

magnitude greater than the 860 (0.04% of 2 million) listed as

extinct by IUCN (2016). The biodiversity crisis is real.

Additional Keywords Amastridae, biodiversity crisis, bivalves,

Euglandina, Gambier Islands, Hawaii, IUCN, Melanopsis ,

Mollusca, non-marine, Powelliphanta , Rhachistia aldabrae.

Red List , snails

INTRODUCTION

Over a decade ago, Lydeard et al. (2004) published a key

paper outlining the decline of non-marine mollusks, the

threats they face, and the high level of extinction com¬

pared with other major animal groups that had been

documented as of 2002 by the International Union for

Conservation of Nature on its Red List. The Red List

program was initiated in 1964 and mollusks were first

included in it in 1983, when 28 species were listed as

extinct (Wells et al., 1983). The Red List only considers

extinctions in modern historical times, from around the

year 1500. Following the realization that an ill-conceived

biological control program had caused the extinction in

the wild of the entire fauna of partulid tree snails on the

island of Moorea in French Polynesia (Murray et al.,

1988), more effort was put into documenting mollusk

extinctions on the Red List. A Moorean partulid appeared

on the front cover of the 1990 Red List (IUCN, 1990), and

when the 1994 Red List (Groombridge, 1994) was pub¬

lished, 255 species were listed as extinct. The number has

gradually increased and the most recent Red List (IUCN,

2016) lists 297 mollusks as Extinct out of a total of 860

extinct species listed.

If we accept a figure of 2 million described species

(Chapman (2009) estimated 1.9 million, and USE (2017)

documents a current yearly increment of around 18,000

newly described species; the Red List accepts 1,736,081

species), this means that between one and two species

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THE NAUTILUS, Vol. 131, No. 1

liave gone extinct per year since 1500, the year from

which IUCN starts counting, or about 0.8 species extinc¬

tions per million species years (E/MSY). The background

rate, based on the fossil record, is around 0. 1-2.0 E/MSY

(Ceballos et ah, 2015). That the rate documented by

IUCN is within the estimated range of the background

rate has provided support for the suggestion by environ¬

mental skeptics (e.g., Lomborg, 2001) that there is no

“Biodiversity Crisis”, despite the views of many scientists

and the media publicity surrounding the notion of the

“Sixth Extinction”, caused by human activities (Novacek,

2001; Leakey and Lewin, 1996). So the question becomes,

is there really a crisis or is it a false or exaggerated claim

by environmental activists and scientists with an arguably

political agenda?

The key question to ask in trving to resolve this con¬

flict is: how accurate really are the IUCN extinction

data? This review summarizes the approaches that have

been developed since the review of Lydeard et al. (2004)

and that have attempted to begin to answer this question

(Regnier et al., 2009, 2015a). It updates the assessments

of Regnier et al. (2009) and reviews a case study of a

Hawaiian land snail family, the Amastridae, that used

these new approaches to obtain a realistic assessment

of extinction (Regnier et al., 2015b).

IS THE IUCN RED LIST APPROPRIATE FOR

ASSESSING EXTINCTION RATE?

The IUCN lias assessed 85,604 species (IUCN, 2016).

This represents a huge amount of detailed work by ded¬

icated biologists, but nonetheless represents only 4.3%

of the total 2 million animal and plant species. Although

a small sample of overall biodiversity, if it were a random

sample, some confidence could perhaps be placed in

its assessment of extinction rate. However, it is not a

random but a highly biased sample.

IUCN (2016) estimated that there are 5,567 known

mammal species and 11,121 known bird species, total

16,688, although Chapman (2009) estimated 5,487 and

9,990, total 15,477, probably a result of differing taxo¬

nomic treatments and estimation protocols. IUCN

(2016) has assessed all mammal and bird species that it

recognizes. Of these, only 849 (~ 5%) were placed in the

IUCN category “data deficient”, that is, they lacked suf¬

ficient information to assess their conservation status

according to the IUCN Red List Categories and Criteria

(IUCN, 2012). Thus, the number of extinctions (239)

listed for mammals and birds by IUCN (2016) is proba¬

bly quite accurate.

However, the situation is very different for inverte¬

brates, which constitute > 95% of described animal

diversity, about 1.31 million (IUCN, 2016) or 1.5 million

species (1.36 million of Chapman (2009) extrapolated

by an annual increment of 1%). Only 18,609 of these

species have been assessed, 1.2% of the total, with 7,205

(39%) of these deemed data deficient. Why is this? There

are two main reasons: 1) taxonomic bias, and

2) the related relative difficulty of obtaining adequate

data to assess the conservation status of invertebrates

compared to vertebrates according to the IUCN criteria.

Taxonomic Bias

There are on average many specialists able to assess the

conservation status of each mammal or bird species. As

most mammal and bird species have been discovered

and described, these specialists are primarily field biolo¬

gists working on ecology, population biology, behavior,

etc. In contrast, most invertebrate specialists are taxono¬

mists or systematists (in the broad sense including those

studying biogeography, phylogenetics, and the assess¬

ment of biodiversity), and most of these systematists

each deal with tens to hundreds of species. There are

roughly equal numbers of specialists focused on verte¬

brates, on plants and on invertebrates, yet plant species

are roughly ten times, and invertebrates a hundred

times, more numerous than vertebrates (Gaston and

May, 1992; May, 2011).

This bias and the 100-fold greater relative number of

vertebrate specialists compared to invertebrate special¬

ists is reflected in the numbers oflUCN Species Survival

Commission Specialist Groups focused on particular

taxa: 73 for vertebrates and only 12 for invertebrates,

with only one for the entire phylum Mollusca (Table 1).

In contrast, many of the vertebrate Specialist Groups

are focused on just one or a few species (e.g., African

elephant, hyaenas, vultures, pelicans, etc.).

IUCN Criteria

The IUCN criteria are detailed and complex. They

include precise quantitative determinations of remaining

numbers of individuals, life history details, area occupied,

Table 1. Number of IUCN Specialist Groups for animals.

R.H. Cowie et al., 2017

Page 5

trends in abundances and range and many other param¬

eters that are precisely defined. This detail and precision

was developed by IUCN in response to criticism that its

assessments were too qualitative and subjective, indeed

secretive (e.g., Mrosovsky, 1997). All mammal and bird

species have been evaluated based on these stringent

criteria, with very few species considered Data Defi¬

cient. This has been possible because, as explained

above, there are many specialists in the field generating

the kind of data that are required.

In contrast, for the great majority of invertebrate

species, few data relevant to the IUCN criteria exist

other than what are available in the original descriptions

(type localities and little else) and perhaps a small number

of subsequent publications. Most of the field research of

any relevance is undertaken as part of biodiversity inven¬

tories, the discovery and subsequent description of the

vast number of species as yet unknown to science, or

indeed to humanity.

MOLLUSKS ASSESSED BY IUCN

The most careful estimate of the number of described

mollusk species (Rosenberg, 2014) suggested that there

are 70,000-76,000, although IUCN (2016) estimated

85,000, following Chapman (2009). Compared to other

invertebrate groups, a relatively high proportion of mol¬

lusk species has been assessed: 7,276 species (IUCN,

2016), or roughly 8.5-10%. However, in contrast to mam¬

mals and birds, a high proportion of these species was

assessed as Data Deficient (2,463 species, 34%), for lack

of adequate information addressing the IUCN criteria.

The Red List (IUCN, 2016) lists 860 species

(744 animals, 1 16 plants) as Extinct, including 297 mollusk

species. Mollusks, despite the small proportion of them

that has been assessed, thus represent 35% of all species

extinctions and 40% of animal extinctions, as reported

by IUCN.

ALTERNATIVE APPROACHES TO ASSESSING

MOLLUSK EXTINCTIONS

Recmer et al. (2009)

Given the shortcomings of the Red List in assessing the

level of extinction of invertebrates overall, alternative

approaches have been sought. Regnier et al. (2009)

re-evaluated mollusk species listed as Extinct on the

Red List of 2007 based on a review of the literature and

by asking a cadre of biologists with expert knowledge to

provide their opinion on the veracity of the Red List

assessments. This literature review and gathering of

expert knowledge also identified additional species not

on the Red List but either documented in the literature

as extinct or simply known to the experts as extinct. Some

of the species listed as extinct were considered in fact

not to be so, either because they had been found alive

since being listed, or because they had been synonymized

with extant species; and two species were excluded as

being nomina dubia. Despite this reduction, from 302

species listed to 269 considered in fact to be extinct,

overall the number of species considered extinct (both

listed and not) increased to 533, including those consid¬

ered Extinct in the Wild (13) and those considered

“possibly extinct” (71) (Regnier et al., 2009: Supporting

Information online), roughly twice as many as correctly

considered Extinct on the Red List. Regnier et al. (2009)

also listed 33 subspecies (including 5 extinct in the wild

and 1 possibly extinct), for a total of 566 taxa.

Update of Regmer etal. (2009)

Following the same approach as that of Regnier et al.

(2009), i.e., literature search and expert consultation (see

the Acknowledgements for the names of the experts

who provided information), we have updated the list of

species considered extinct. We took the most recent

evaluation of each species as representing its current

status, which was either the most recent IUCN evalua¬

tion as listed in the Red List (IUCN, 2016), Regnier et al.

(2009), or our own literature/expert consultation. We

excluded species listed as Extinct, Possibly Extinct, or

Extinct in the Wild on the Red List and/or by Regnier

et al. (2009) if they are now thought to be extant

(Appendix Table Al). We also did not consider subspe¬

cies, neither those recognized in the Red List nor those

listed by Regnier et al. (2009). Subspecies and synonyms

that have been recognized in the literature subsequently

but that are still retained as valid species on the Red List,

as well as undescribed species listed with provisional

names on the Red List, were also excluded (Appendix

Table A2).

Of the 297 species listed as Extinct on the Red List,

we considered six as now only Possibly Extinct, three

as Extinct in the Wild, 20 as extant, and 1 1 that have now

been considered synonyms, subspecies, nomina dubia,

or unrankable. Of the 124 listed as “Critically Endan¬

gered (Possibly Extinct)” on the Red List, three are

known to he extant, six are considered as now extinct,

with a further five (Galapagos Bulimulus species)

undescribed, five synonymized, and five unrankable.

And of the 14 listed as extinct in the wild, we considered

one to be extant in the wild and five to now be extinct.

Thus, excluding undescribed species and species still

listed as valid on the Red List hut that have been synon¬

ymized, reduced to subspecies, considered unrankable,

or are now thought to be extant, the current Red List

(IUCN, 2016), in our view correctly lists 386 valid spe¬

cies in the combined categories of Extinct, Critically

Endangered (Possibly Extinct), and Extinct in the Wild,

which is 44 species fewer than the 430 actually listed by

IUCN (Table 2).

The additional information derived from the literature

search and expert consultation allowed us to estimate

that in fact 638 species are extinct, 380 possibly extinct

(EX?), and 14 extinct in the wild, a total of 1,032 species

in the combined categories (Appendix Tables A3-5).

Page 6

THE NAUTILUS, Vol. 131, No. 1

Table 2. Numbers of mollusk species considered extinct

(EX), critically endangered (possibly extinct) (CR(PE)), and

extinct in the wild (EW) in the Red List (IUCN, 2016), with

species on the Red List re-assessed herein, and the results of

the present study based on additional literature search and

expert consultation.

1 Includes 1 1 fossil/subfossil species listed as extinct

"includes 46 fossil/subfossil species listed as extinct

3CR(PE) in the Red List, EX? in this study

Of these, 47 are known only as “fossil” or “subfossil” but

in many of these cases it was not possible to say when

they went extinct, perhaps in some cases from natural

causes such as non-anthropogenic climate change. For

comparability with the approach officially taken by

IUCN of focusing on species that have gone extinct since

around the year 1500 (though 11 fossil/subfossil species

are included in the Red List), we might conservatively

exclude the 47 fossil/subfossil species in our list and then

would consider 591 species as extinct, 380 as possibly

extinct, and 14 as extinct in the wild, total 985 species.

Even so, our numbers of extinct and possibly extinct

species both greatly exceed those of the Red List, by

more than two and three times respectively. This total is

also approximately double the number listed by Regnier

et al. (2009).

Of the 1,032 species (Appendix Tables A3-5), 803 are

land snails, from 52 families but dominated by species of

four Pacific island families, the Amastridae (307 species),

which is a Hawaiian endemic family (see below),

Endodontidae (92 species), Partulidae (52 species) and

Achatinellidae (44 species), as well as one more wide¬

spread family (though with greatest diversity in the

Pacific), the Charopidae (54 species). Freshwater

snails are represented by 177 species from 22 families,

with all but two families (Hvdrobiidae, 61 species;

Pleuroceridae, 32 species) represented by 12 or fewer

species. Freshwater bivalves are represented by

46 species from five families, with only the Unionidae

(40 species) having more than one or two species. Six

marine gastropods are listed.

Regnier et al. (2015)

Regnier et al. (2009) and the updated assessment pro¬

vided above, have only dealt with species already assessed

by IUCN and those additional species that were known to

be extinct, possibly extinct, or extinct in the wild, both

documented in the literature and as known to biologists

with expert knowledge. These species were therefore not

a random sample. A more realistic estimate of the true

number of mollusk extinctions would only be provided by

assessing a random sample of mollusk species.

Therefore, Regnier et al. (2015a), focusing on land

snails, generated a rigorously random sample of 200 spe¬

cies from a wide representation of localities across the

globe. They evaluated these species based on the IUCN

categories and criteria (IUCN, 2012) by reviewing the

literature as well as major museum collections. For com¬

parison with this IUCN-based evaluation, they also sent

the list of 200 species to numerous land snail experts,

asking them to evaluate whether those species for which

they had personal knowledge and experience were

extinct. For species for which no expert was available,

Regnier et al. (2015a) made their own assessment based

on collection records. In addition, Regnier et al. (2015a)

developed a mathematical probabilistic model, based on

collection dates as documented in major museum mala-

cological collections. This model evaluated the probabil¬

ity of extinction for each of the 200 species, and thereby

offered an independent means of corroboration (or not)

of the expert evaluation.

Based on the IUCN categories and criteria, Regnier

et al. (2015a) were only able to evaluate 31 of the 200 spe¬

cies, the other 169 being categorized as Data Deficient.

Of the 31, three (1.5% of the 200, but 10% of the evalu¬

ated 31 ) were evaluated as extinct. Under the assumptions

that the 200 land snail species in the random sample are

representative of the described non-marine molluscan

diversity — roughly 30,000 species (Rosenberg, 2014) —

and that marine molluscan extinction is negligible com¬

pared to non-marine extinction (e.g. Carlton, 1993; but

see Peters et al., 2013), extrapolation leads to an estimate

of 3,000 extinct mollusk species.

In contrast, the experts were able to evaluate 118 of the

200, the remaining 82 being “Impossible to Assess”.

Twenty (10% of the 200, but 17% of the evaluated 118)

were evaluated as extinct. Note that Regnier et al. (2015a)

used slightly different terminology from the IUCN

categories in order to draw attention to the differences

between the two approaches. The probabilistic model

broadly corroborated the expert evaluations in terms of

the proportion of species considered extinct.

Of the 76,000 described mollusk species (Rosenberg,

2014), about 46,000 are marine (WoRMS, 2017) and

roughly 30,000 non-marine. Therefore, as 10-17% of

the 200 land snail species were considered extinct,

extrapolation suggests that in fact around 3,000-5,100

mollusk species are extinct, far more than the 297 on the

Red List (IUCN, 2016), the 532 estimated by Regnier

et al. (2009), the 1,032 estimated above updating Regnier

et al. (2009), but in the same region as the 3,000 extrapo¬

lated from the assessments of Regnier et al. (2015a) based

on the IUCN categories and criteria. This estimate of

3,000-5,100 mollusk extinctions, even taking into account

that it is based on a small sample, is shocking. And many

are going extinct before they have been discovered and

described (e.g., Richling and Bouehet, 2013; Sartori et al.,

2013; 2014).

R.H. Cowie et al., 2017

Page 7

WHY ARE NON-MARINE MOLLUSKS

GOING EXTINCT?

There are at least four possible causes of non-marine

mollusk extinction, which are, for the most part, the same

causes of the extinction of non-marine species in general:

habitat destruction, impacts of introduced species, exploi¬

tation and collecting, and, potentially, climate change.

Habitat Destruction

Urbanization, deforestation, agricultural expansion and

exploitation of natural resources have all had impacts

on mollusks. Three examples serve to illustrate some of

these threats.

Gambler Island Land Snails: Based on collections

made by the Bishop Museum (Honolulu) Mangarevan

Expedition in 1934 and bv the Museum national

d’Histoire naturelle (Paris) in 1997, 46 endemic species

have been recorded from the Gambier Islands in the

families Euconulidae, Endodontidae, Assimineidae, and

Helicinidae (Abdou and Bouehet, 2000; Bouchet and

Abdou, 2001; 2003; Bidding and Bouchet, 2013). Only

three of these species were still extant; the remainder

were described from empty shells collected from the

shell bank of the soil.

The cause of the extinction of almost this entire fauna

was deforestation (Ridding and Bouchet, 2013). Defor¬

estation began with the first arrival of Polynesian settlers

around 1,000 years ago and reached a peak in the 17th

and 18th centuries with the total destruction of the

native flora (Conte and Kirch, 2008), no doubt exacer¬

bated after the arrival of Europeans in the early 19th

Century. A few of the snail species were still extant in

the 1840s-1860s, but no living specimens of all but the

three known to be extant have been collected since the

19th Century (Ridding and Bouchet, 2013). Similar sce¬

narios have played out across the islands of the Pacific.

Melanopsis parreyssii in Romania: This freshwater

species was listed as Critically Endangered on the Red

List in 2013 (Feher, 2013). It was deemed Extinct in

the Wild in 2016 (STrbu and Benedek, 2016). It was

extremely narrowly endemic in Romania but had also

been introduced to Hungarv and Bulgaria. However, by

2010 these introduced populations had vanished (Feher,

2013; STrbu et ah, 2013). The Romanian locality was part

of a system sustained by a geothermal aquifer that was

declared a nature reserve and a Natura 2000 Site of

Community Importance. There were lakes and creeks

fed by thermal springs, forming the only habitat of

Melanopsis parreyssii. However, rapidly increasing recent

development of the geothermal waters, especially for tour¬

ism, led to the springs becoming clogged and the natural

thermal lakes diminished, up to the point where the only

natural, but shrinking, hike that remained was Pejea

(referred to as Bade Episcopiei bv Feher, 2013). By 2011

the spring serving Pejea Lake ceased activity and by 2015

the lake had become little more than a puddle supporting

no mollusks except an invasive bivalve (STrbu et ah, 2013;

STrbu and Benedek, 2016). Captive breeding efforts have

met with little success (STrbu and Benedek, 2016). Human

greed and disregard for the environment, including laws

supposedly protecting it, had led to the destruction of

the habitat of this narrowly endemic species and thus

its extinction.

Poivelliphanta augusta in New Zealand:

Powelliphanta species are large predatory, worm-eating

land snails endemic to New Zealand and most have very

small ranges, making them highly vulnerable to habitat

destruction (Walker et ah, 2008; Boyer et ah, 2013). A

species of Powelliphanta , first collected in 1996 but not

recognized as a possible new species until 2003, and

confirmed as such by Trewick (2005), was discovered on

Mount Augustus, a peak on the Stockton Plateau in

New Zealand’s South Island and the site of a large open

cast coal mine (Trewick et ah, 2008). By 2003, much of

the snails’ habitat had been destroyed, with the entire

remaining 8.5 ha of ridge-top habitat under severe threat

from the mining. With this imminent threat, and follow¬

ing legal action (see Walker et ah, 2008; Boyer et ah,

2013), all snails and eggs that could be found were col¬

lected and brought into captivity, beginning in 2006.

Soon thereafter, all but a tiny piece of snail habitat was

destroyed (Walker et ah, 2008). Many of the snails were

transferred back to the wild at three sites with sup¬

posedly similar habitat, but the mortality rate in these

populations was such that they were unlikely to survive

(Morris, 2010). One of these sites was created bv trans¬

ferring entire habitat from the original site to an area not

slated to hie mined, but the large trees did not survive

well and the habitat was invaded by weedy species

(Morris, 2010). The captive snails exhibit slower growth

and higher hatchling mortality than estimated in the orig¬

inal wild population (James et ah, 2013). Furthermore, a

large proportion of the captive snails died following an

electrical malfunction in their temperature-controlled

facility (James et ah, 2013). The species was described as

Poivelliphanta augusta in 2008 (Walker et ah, 2008).

Although P. augusta is not yet extinct, the destruction of

its entire habitat by coal mining has left it on the brink.

Impacts ok Introduced, Species

It is generally difficult to demonstrate definitively

that an invasive species has caused the extinction of

another species. For example, following the zebra mussel

( Dreissena polymorpha) invasion of North America

beginning around 1 985, many of the native freshwater

mussels (Unionoida) were thought to be doomed

(Ricciardi et ah, 1998). At localities with high densities

of D. polymorpha , local populations of native mussels

were being extirpated and some of the native species

were in steep decline or becoming regionally extinct.

Over 60 species were thought to be in danger of global

extinction from the combined effects of zebra mussels

and habitat degredation (Ricciardi et ah, 1998). However,

Page S

THE NAUTILUS, Vol. 131, No. I

a decade later, Strayer and Malcom (2007), focusing on

four species in the Hudson River, showed that although

they had declined steeply following zebra mussel inva¬

sion, by 2000-2004 populations of these species had

stabilized at 4—22% of their pre-invasion densities, offering

a slender hope that the native mussels might be able to

co-exist with the invaders, albeit at much lower densities

(Strayer and Malcom, 2007).

In contrast, the prime example of an invasive species

causing extinction of mollusk species is the introduction

of the predatory snail Euglandina rosea to the islands of

the Pacific, notably to the Hawaiian Islands and the

Society Islands of French Polynesia but also elsewhere

(e.g., Cowie and Cook, 2001), in poorly considered

efforts to control the invasive giant African snail,

Achatina fulica (Hadfield, 1986; Murray et ah, 1988).

The clearest evidence of a direct impact was that as

E. rosea spread across the island of Moorea, the endemic

Partula tree snail species vanished in its wake; it did not

control A. fulica (Murray et ah, 1988; Cowie, 2001). On

the other islands of the Society group the same story

played out (Coote and Loeve, 2003; Gerlaeh, 2016).

In Hawaii, the combination of E rosea and invasive

rats, following on from habitat destruction, has caused

the decline of endemic achatinelline tree snails (Hadfield

et al., 1993), and another introduced predatory snail,

Oxychilus alliarius, may yet impact endemic Hawaiian

species, notably the single species in the endemic mono-

typic helicarionid genus Koala (Curry et ah, 2016). The

invasive predatory flatworm Platydemus inanokwari has

caused the extinction of endemic Pacific island snails,

notably in the Ogasawara Islands (Chiba and Cowie,

2016). Competition between invasive and native snails

may also be important, but no definitive instances of this

have been documented (Cowie, 2005).

The impacts of invasive species are often inextricably

linked to those of habitat destruction or modification, as

invasive species, such as rats (e.g., Athens, 2009), may

drastically alter habitat, and habitat alteration may facil¬

itate the spread of invasive species (Didham et ah, 2007).

As such, they can be at least the partial cause of extinc¬

tion. However, invasive species may act in concert with

or consecutively with habitat alteration, making it diffi¬

cult, with some clear exceptions, to say that invasive

species, per se, have been the cause of specific mollusk

species extinctions.

Exploitation and Collecting

Numerous non-marine mollusk species are exploited for

human consumption. In Europe, and especially in coun¬

tries bordering the Mediterranean, various of the larger

species of land snails are collected and eaten, most nota¬

bly Helix pomatia , the “escargot de Bourgogne”, and

Cornu aspersum , the “petit gris”, both of which are read¬

ily available in most French markets, but also more

widely. However, although C. aspersum remains abun¬

dant and widespread in western Europe, H. pomatia lias

declined, notably in France, and efforts are increasingly

being made to culture it for export, especially in eastern

Europe (Ligaszewski et ah, 2007). Nonetheless, H. pomatia

is listed as of Least Concern on die Red List (IUCN, 2016).

Various other species are eaten around the Mediterranean

(Yildirim et al., 2004) but none seems to have attracted

conservation concern. The collection in the wild for the

restaurant trade, in combination with habitat loss and

alien species, has endangered the endemic “bulimes”

(genus Placostylus) of New Caledonia (Brescia et ah,

2008; Neubert et ah, 2009). In Asia, various species of

Ampullariidae, Viviparidae, and Pachychilidae in partic¬

ular are eaten, as are a number of clams and mussels

(e.g., Kohler et ah, 2012), and Achatinidae are eaten in

West Africa (e.g., Nyoagbe et ah, 2016); but none of

these species has attracted great concern because of this.

There are a few records of land snails being used for

medicinal purposes, e.g., Theba pisana (Benitez, 2011)

and Achatina fulica (Cowie and D.G. Robinson, 2003),

and religious purposes, e.g., Achatina fulica (Neto et ah,

2012), and they may be a significant part of local rural

economies (Osemeobo, 1991); they may also be intro¬

duced beyond their native range for such religious pur¬

poses (Vazquez et ah, 2016). But there is no evidence

that these usages have led to the decline and certainly

not extinction of these species.

In the 19th Century, freshwater mussels (Unionida)

were commercially harvested for their pearls, notably in

the United States; over-harvesting led to decline of

the populations and the fishery was largely abandoned

(Neves, 1999; Anthony and Downing, 2001). H owever,

soon thereafter, the demand for shells of freshwater

mussels for the button industry burgeoned, causing fur¬

ther declines and adding to the already serious and

increasing threats from habitat degradation; but this

industry essentially died out with the advent of plastics

(Neves, 1999; Anthony and Downing, 2001; Strayer

et al., 2004), although it persists in other parts of the

world (Beasley, 2001). However, the discovery in Japan

that mussel shell material could act as nuclei for the

production of cultured pearls, resulted in a further

phase of exploitation of mussels in the United States for

export, although demand declined drastically by the late

1990s (Neves, 1999) Although habitat degradation has

been generally considered the primary cause of mussel

decline, over-exploitation has also been important (Strayer

et al., 2004).

The hobby of shell-collecting is generally more

focused on marine than on non-marine species, with

some marine taxa, for instance in the genus Conus ,

threatened as a result (Peters et al., 2013). Nonetheless,

among non-marine species there are a few notable

instances in which shell collecting and ornamental use

may have been at least in part responsible for the decline

and perhaps extinction of certain species (Cowie, 2004).

Most notably, collecting of snails by late 19th and early

20th Century shell collectors quite possibly had an

important impact on some of the larger and more colorful

Hawaiian species, primarily but by no means exclusively

the beautifully colored and patterned Achatinellinae

R.H. Cowie et al., 2017

Page 9

(Hadfield, 1986). Compared to marine species, there is a

much more limited collectors’ trade in shells of non-

marine species, which nonetheless may lead to endanger-

ment. However, the legal instruments of control (notably

the Convention on International Trade in Endangered

Species (CITES)) list only three non-marine gastropod

genera: the genus Achatinella , with 39 species listed as

Extinct or Critically Endangered by 1UCN (2016), the

genus Polymita , with no species listed, and Papustijla

pulcherrima , the Manus Island (off the north coast of

New Guinea) green tree snail, which is listed as Near

Threatened by IUCN (2016) (see also Whitmore, 2016).

The collection of the 10,000 or so shells of the partulid

tree snail Eua zebrina that once made up the chandeliers

in the lobby of American Samoa’s then main hotel surely

must have significantly reduced at least some populations

of that species (Cowie, 1993).

Overall, therefore, exploitation and collecting have not

been a major cause of mollusk extinction, with a number

of notable exceptions.

Climate Change

Gerlach (2007) declared that Rhachistia aldabrae, an

endemic cerastid from Aldabra Atoll that was still locally

abundant in the 1970s (Gerlach, 2009), had gone extinct

in the late 1990s as a result of declining rainfall. It was

therefore placed on the Red List as Extinct (Gerlach,

2009). This is the only instance of a mollusk being

reported as having gone extinct as a result of climate

change. However, in 2014 it was discovered alive

(Battarbee, 2014). Nonetheless, there is only one tiny

population (|. Gerlach, pers. comm.) and it seems likely

that with ongoing climate change it may yet succumb.

The Red List (IUCN, 2016) has not yet been updated.

Baur and Baur (1993) concluded that the local extir¬

pation of the widespread European land snail Arianta

arbustorum at sites around the city of Basel, Switzerland,

had resulted from climate warming in otherwise suitable

areas close to extensive urban development, and that

sites from which A. arbustorum had disappeared had

higher surface temperatures than sites where it remained.

The same authors (Baur and Baur, 2013) compared

historical records from 1916-1917 with survey results

from 2011-2012 on nine mountain slopes in Switzerland.

They found that the upper elevational limit for A.

arbustorum had risen 164 m in the 95 year period, during

which mean annual temperature in the area had risen

1.6 °C. Although only a local impact, this study demon¬

strated the potential for climate change to affect popula¬

tions of land snails.

Similarly, Pearce and Paustian (2013) undertook

extensive elevational surveys in Pennsylvania, USA, to

assess whether, with climate warming, species forced

ever upward would eventually have nowhere further to

retreat to (ef. similar studies on arthropods: Meyer et ah,

2015). Of the 69 species recorded, five appeared espe¬

cially susceptible. This kind of susceptibility is of partic¬

ular concern on oceanic islands, especially in the Pacific.

On many Pacific islands, habitat destruction and the

introduction of invasive species at lower elevations has

resulted in most of the remaining endemic land snail

species being confined to higher elevation refugia

(Durkan et al., 2013), either because their lower eleva¬

tion populations have been extirpated or because they

are evolutionarily adapted to the lower temperatures

at these higher elevations and historically only ever

occurred there. As such, with limited opportunity to

move to higher elevations as the climate warms, they

face extinction.

Thus, there is no evidence that climate change has

caused the extinction of any non-marine mollusk species.

However, continued warming will probably have more

serious effects in the future, and ocean acidification

resulting from raised carbon dioxide levels may impact

marine species (Peters et al., 2015).

EXTINCTION ON PACIFIC ISLANDS:

A CASE STUDY

Among the species assessed as extinct by Regnier et al.

(2009), more than 70% were from oceanic islands and

most of these were from the Hawaiian Islands, French

Polynesia and the Mascarene Islands. Previous authors

have suggested that 65-90% of the Hawaiian land snail

species have gone extinct (Solem, 1990; Cowie and A.C.

Robinson, 2003; Lydeard et al., 2004). The proportion

differs among families, but three groups (Achatinellinae,

Amastridae, Endodontidae) appear to have suffered

“catastrophic extinction” (Solem, 1990; and see above).

To begin to get a more accurate assessment of the level

of extinction in Hawaiian land snails, Regnier et al.

(2015b) focused on the Amastridae, a family endemic to

the Hawaiian Islands and with 325 known valid species

(Cowie et al., 1995). Rather than using the rigid IUCN

categories and criteria (IUCN, 2012), they took a less

rigorous approach similar to that taken by Regnier et al.

(2015a). They based their assessments on a comparison

of information from historical collections and archived

field notes in the Bishop Museum, with data from

modern extensive surveys undertaken throughout the

Hawaiian Islands by K.A. Hayes, N.W. Yeung, and col¬

laborators between 2004 and 2013. They also consulted a

diversity of experts with experience in the Hawaiian land

snail fauna. A species was considered extinct if it had not

been found since 2004 at any recently surveyed location

where it had formerly been recorded. In addition, and

again taking a similar approach to that adopted by

Regnier et al. (2015a) in order to provide independent

corroboration, Regnier et al. (2015b) undertook a statis¬

tical assessment of extinction probabilities, based on

collection years and using the methods of Thompson

et al. (2013) and Lee (2014).

Of the 325 species, 131 were assessed as extinct; there

was insufficient evidence of extinction for 179, although

most of these can probably be considered extinct (and

were considered possibly extinct in the updated analysis

Page 10

THE NAUTILUS, Vol. 131, No. 1

of global extinctions, above); but only 15 were considered

definitively extant (three subsequently found extant;

N. W. Yeung and K.A. Hayes, pers. comm.). Thus, a

minimum of 131 (40%) and maximum 310 (95%) were

considered extinct. The probabilistic assessment was

consistent with the expert assessment: the probabilities

of being extant for those species assessed as extinct

was <0.01 (111 species), <0.1 (16 species) and 0. 1-0.3

(4 species); and for those species assessed as extant it was

O. 38-0.93 (15 species); the species for which there was

insufficient evidence of extinction were not assessed

probabilistically. The Red List (IUCN, 2016) lists only

33 amastrid species (10%) as extinct.

There have been five phases of amastrid extinction,

discussed in more detail by Regnier et al. (2015b),

as follows.

1) Description as fossils or subfossils and not known to

be extant, but it is not possible currently to determine

when they went extinct, i.e., prior to or after human

colonization of the Hawaiian Islands, or prior to or

after around the year 1500.

2) Subsequent to the first colonization of the islands

by Polynesians, 800-1000 years ago, which led to con¬

siderable habitat destruction and introduction of a

number of alien species.

3) Following European colonization, when extensive

additional habitat destruction took place and highly

destructive invasive alien species were introduced.

4) Following the advent of large-scale agriculture at the

end of the 19th Century, at the time of a major

increase in land snail extinction rate globally, identi¬

fied as around 1895 by Regnier et al. (2015a).

5) After 1945 and the end of the Second World War, with

the increased military activity, tourism, commerce,

urbanization and rapidly increasing introduction of

invasive species, including snails (Cowie, 1998).

If the extinction rate were constant over this roughly

1 ,000 year period, it would have been between roughly

0.4 and 1 .0% of the fauna per decade, given the extremes

of 131 and 310 of the 325 amastrid species having gone

extinct. However the rate was certainly not constant but

probably has increased in a roughly exponential and

step-wise manner over time. Regnier et al. (2015b)

therefore modeled a number of scenarios reflecting this

increasing rate. The overall rates obtained ranged from

0.4% of the amastrid fauna per decade (131 species

extinct, beginning in the year 1000, as above) to 14%

per decade (310 species extinct, beginning in 1945).

These scenarios are certainly over-simplistic, but none¬

theless provide a framework for discussion.

DISCUSSION

The most conservative estimate of 0.4% per decade for

the Hawaiian amastrid extinction rate is similar to the

global biodiversity extinction rate of < 1% per decade

estimated by Costello et al. (2013). However, this extinc¬

tion rate is probably not reflective of the true rate of

amastrid extinction, as not only is it based on a very

conservative estimate of the number of species that have

gone extinct (131) hut it assumes a constant rate since

the year 1000. Undoubtedly, the rate has increased over

the millenium and Regnier et al. (2015h) suggested

that a rate of around 5% per decade over the last 1 50—

200 years would he more realistic, indeed still rather

conservative, given the maximum rate they estimated

of 14% per decade. A rate of 5% would lead to a loss of

> 50% of a fauna within 150 years (Costello et al., 2013).

Indeed, for the amastrids, with only 18 of 325 species

known to be extant (i.e., including the three species

discovered alive since Regnier et al., 2015b; see above),

this scenario seems to have already played itself out.

This rate (5% per decade) is much higher than the

global estimate of the loss over the last 500 years or so

of 3,000-5,100 (10-17%) of the 30,000 known land snail

species, as estimated by Regnier et al. (2015a) and out¬

lined above. The amastrids, however, may be an extreme

case, although land snail groups from other Pacific

islands have suffered similar fates, notably the

Endodontidae (Solem, 1976; Zimmerman et al., 2009;

Sartori et al., 2013; 2014) and Partulidae (Coote et al.,

2003; Gerlach, 2016), and many extinct species continue

to be found, as empty shells, even before their scientific

description (e.g., Richling and Bouchet, 2013). Oceanic

island biotas are in general much more susceptible

to extinction than more buffered continental faunas

(Triantis et al., 2010). And some taxa may be more sus¬

ceptible than others. Therefore it may be dangerous to

base generalizations regarding extinction rates on global

estimates, though even these, such as the loss of 10-17%

of land snail species in 500 years described here, are

cause for great concern. While it is crucial to increase

awareness of the high level of global extinction, subsum¬

ing more local extinction rates, especially of particularly

susceptible faunas such as those of oceanic islands, or of

particularly susceptible taxa such as the Amastridae,

under global rates will doom those plants and animals

to extinction as their special vulnerability and need

for conservation will be overlooked, or at least not

adequately appreciated.

If we assume that L) the 200 land snail species

sampled by Regnier et al. (2015a) are representative

of known non-marine invertebrate diversity and their

extinction rate, 2) three-quarters of species are non¬

marine (Mora et al., 2011), and 3) marine extinctions

are negligible compared with non-marine extinctions

(only four marine mollusks are considered as extinct;

IUCN (2016), and see above), then approximately 7.5-

13% of all species have gone extinct since around 1500.

This is orders of magnitude greater than the 860 (0.05%

of 2 million) listed as extinct by IUCN (2016). The bio¬

diversity crisis is real.

But what of the IUCN? The studies reviewed herein

have shown that it is inappropriate to use the IUCN Red

List as a source of data on global extinction rates (except

for mammals and birds), and more generally that

R.H. Cowie et al., 2017

Page 1 I

assessing overall levels of threat to all biodiversity based

on the species listed by IUCN seriously downplays that

threat, notably because the great majority of biodiversity

(invertebrates) has not been evaluated. A similar critique

was voiced by Possingham et al. (2002), who argued that

threatened species lists (such as the IUCN Red List )

should not be used to indicate the overall status of bio¬

diversity and changes in it, largely because of uneven

taxonomic treatment and variation in observational effort

(as described above for vertebrates compared to inverte¬

brates). Nonetheless, IUCN is the premier and most

influential global conservation organization. But its goal

is to "highlight taxa threatened with extinction, and

thereby promote their conservation” (IUCN, 2016);

documenting extinction is incidental to this goal as once

extinct a species cannot be conserved. For terrestrial

vertebrates IUCN is well on the way to achieving its goal,

but invertebrates present a daunting challenge both

because of their immense diversity and because of the

lack of adequate data to apply the IUCN criteria for the

vast majority of them.

Major focused efforts by IUCN continue to be made

to evaluate additional mollusk species (e.g., Seddon,

2011; 2014; 2015; Pippard, 2012; Peters et al., 2013;

Seddon et ah, 2014; Allen et ah, 2016; Bolnn and

Allcock, 2016; Neubert et al., 2017). These efforts have

focused on particular taxa, habitats and geographic loca¬

tions that were deemed a priori as especially in need of

attention, i.e., to address the IUCN goals of highlighting

taxa in need of conservation (above), and for which

funding could be obtained. Nonetheless, at the current

rate it will be many years before all mollusks, or even all

non-marine mollusks, have been assessed. The approach

we have taken in the two studies reviewed herein

(Regnier et ah, 2015a, b), as well as our update of the

analysis of Regnier et al. (2009) based on new informa¬

tion, is an attempt to speed up the evaluation process

and to develop a method that allows global trends to be

more realistically determined. Admittedly, our approach

is less rigorous than the process of applying the IUCN

criteria to assign species to the IUCN categories, with

peer review required (when at best only one specialist

lias any knowledge of the fauna), but is considerably

quicker and more cost-effective. While there is a chance

that our approach might incorrectly list some species as

extinct and thereby cut them off from conservation

attention, it has the potential to identify many more

species in need of conservation, species that would be

listed as Data Deficient by IUCN and therefore also

ignored. Our approach also has the advantage that it

can provide a much more realistic overview of the bio¬

diversity crisis than can the Red List , especially regard¬

ing the extraordinary levels of extinction, which was

our immediate focus in the studies reviewed above.

Nonetheless, IUCN remains the preeminent global con¬

servation agency with a crucial role in identifying con¬

servation needs and developing global conservation

strategies. Our efforts do not in any way compromise

those roles.

ACKNOWLE DC M E NTS

We thank our collaborators Amaury Lambert and

Guillaume Achaz (Regnier et ah, 2015a) and Ken Hayes,

Norine Yeung, Carl Christensen, and Daniel Chung

(Regnier et al., 2015b). We also thank all the experts who

contributed information and assessments for those two

studies, the numerous students and others who par¬

ticipated in the Hawaiian survey work, and others who

provided assistance, as acknowledged in those two

publications. This paper is based on a presentation

given by Robert Cowie at the Mollusks in Peril Forum

(Bailey- Matthews National Shell Museum, Sanibel

Island, Florida, May 2016). We thank the organizers of

the Forum, notably Jose II. Leal and Dorrie Hipschman,

respectively Science Director and Executive Director

of the Bailey-Matthews National Shell Museum, and

Museum benefactors Smoky and Stephanie Payson, for

tlie invitation to participate and for funding in support of

that participation. Additional information was provided

by M.R. Alonso, Gary Barker, Rudiger Bieler, Fred

Brook, Robert Cameron, Satoshi Chiba, Carl Christensen,

Zoltan Feher, Justin Gerlach, Jozef Grego, Brenden

Holland, Yasunori Kano, Miguel Ibanez, Ben Rowson,

Rebecca Rundell, Menno Schiltbuizen, Steve Trewick,

and Norine Yeung. We thank Chuck Lydeard for

reviewing the manuscript. This contribution is partly

based on research supported by the French National

Research Agency Losers Project Grant ANR-09-PEXT-

007, an Ars Cuttoli Foundation grant, NSF grant DEB-

1120906 and by grants from the U.S. Department of

Agriculture (CAPS program) and the Oahu Army Natural

Resources Program. Contribution number 9977 of the

University of Hawaii School of Ocean and Earth Sciences.

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Table Al. (cont.)

R.H. Cowie et al., 2017

Page 17

Table A3. Terrestrial species considered extinct (EX), possibly extinct (EX?) or extinct in the wild (EW) in the present study,

compared with their status as evaluated by Regnier et al. (2009), and on the Red List (IUCN, 2016). Red List categories are extinct

(EX), extinct in the wild (EW), critically endangered (possibly extinct) (CR(PE)), critically endangered (CR), and data deficient

(DD); the date of the IUCN evaluation follows the status. EX? is treated as equivalent to CR(PE). A dash indicates the species was

not evaluated. Sources are only provided if the status in this study differs from the later of IUCN (2016) and Regnier et al. (2009).

Species explicitly described as fossil or subfossil are asterisked.

( Continued )

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Table A3, (cont.)

( Continued )

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Table A3, (cont.)

Page 32

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Table A3, (cont.)

R.H. Cowie et al., 2017

Page 33

Table A4. F reshwater species considered extinct (EX), possibly extinct (EX?) or extinct in the wild (EW) in the present study,

compared with their status as evaluated by Regnier et al. (2009), and on the Red List (IUCN, 2016). Red List categories are extinct (EX),

extinct in the wild (EW), critically endangered (possibly extinct) (CR(PE)), critically endangered (CR). least concern (LC), and data

deficient (DD); the date of the IUCN evaluation follows the status. FIX? is treated as equivalent to CR(PE). A dash indicates the species

was not evaluated. Sources are only provided if the status in this study differs from the later of IUCN (2016) and Regner et al. (2009).

Page 38

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Table A4. (cont.)

Table A5. Marine species considered extinct (EX) or possibly extinct (EX?) in the present study, compared with their status as

evaluated by Regnier et al. (2009), and on the Red List (IUCN, 2016). Dashes indicate that the species was not evaluated. A source is

only provided for species of Conidae, for which the status in this study differs from that of IUCN (2016) and Regner et al. (2009).

Species Red List Regnier et al., 2009 This study Source for revised status

R.H. Cowie et al., 2017

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THE NAUTILUS 131(l):43-49, 2017

Page 43

Is mining the seabed bad for mollnsks?

Julia D. Sigwart

Queen’s University Belfast

Marine Laboratory

12-13 The Strand

Portaferry, NORTHERN IRELAND

and

University of California, Berkeley

Museum of Paleontology

VLSB 1101, Berkeley CA 94720 USA

Chong Chen

Department of Subsurface Geobiological

Analysis and Research

Japan Agency for Marine- Earth Science

and Technology (JAMSTEC)

2-15 Natsushima-cho, Yokosuka

Kanagawa, 237-0061, JAPAN

Leigh Marsh

Ocean and Earth Science

National Oceanography Centre

University of Southampton

Southampton, UNITED KINGDOM

ABSTRACT

Up to three miles below the ocean surface, deep-sea hydro-

thermal vents are home to a community of extraordinary mol-

lusks. In an environment without light, under intense pressure

and volcanic heat, many gastropods and bivalves living directly

on the vent chimneys show adaptations that have driven impor¬

tant scientific breakthroughs. For example, the famous “sealy-

foot” gastropod, Chn/somallon squamifenim, has hard scales

on its foot with a crystalline iron coating that has inspired novel

defensive armor designs. This iconic species has only been

reported from three sites in the Indian Ocean, each site hun¬

dreds of miles apart and only around half the size of a football

field. Two of these three sites are already designated under

international exploration licenses for deep-sea mining, to extract

rare minerals from the vent chimneys. Economic and political

pressures to exploit the seabed are advancing much faster than

scientific exploration, putting these vent ecosystems and their

molluscan residents at risk.

MOLLUSKS IN THE DEEP SEA

General perception of marine mollnsks is naturally driven

by our access to shallow marine species commonly found

on beaches and the history of shell collecting. The spe¬

cies and varied ecosystems found in the deep sea are

less familiar to non-specialists.

The deep oceans represent a broad variety of Habitats

and ecosystems, distributed across a three-dimensional

volume of water that represents over 90% of the habit¬

able space on Earth (Costello et al., 2010; Rex and Etter,

2010). Mollusks inhabiting the ocean floor cover its

entire range, from shallow coastal environments to the

deep sea. The characteristics of the deep sea vary geo¬

graphically, for example the depths of thermoclines, inso¬

lation, and lysoclines (depth of carbonate saturation),

vary latitndinally and between ocean basins (Rex et al.

2000; Steele et al. 2009). These physical and chemical

conditions represent specific challenges or adaptive

pressures, which manifest in shell forms that are dis¬

tinctly different than shallow-water species more com¬

monly seen in shell collections: aphotic conditions

below 1000 m or less result in a lack of shell pigmen¬

tation (Abbott, 1985), and calcium limitation at depths

below 3000-4000 m (Morse et al., 2007) results in

typically thin and fragile shells. Aesthetics combined

with the expense and technical challenges of deep-sea

exploration mean that the shells of deep-sea species are,

unusually for mollusks, not generally available on the

commercial market.

Access to study deep-sea habitats principally depends

on large-scale ocean going research vessels equipped

with specialized sampling equipment. Such infrastruc¬

ture is generally only available through support from

government funding of major nations, and indeed most

deep-sea exploration focuses on geology, oceanography,

climate change, and many other aspects besides sam¬

pling benthic animals such as mollusks. The large-scale

investment and funding required, and the rarity of these

samples, ethically demand that all such materials should

be held permanently in public collections and preserved

for further research and education.

The ocean floor remains largely unexplored: perhaps

10% of the seafloor has been mapped by ship-borne

instrumentation and far less lias been sampled biologi¬

cally (Charette and Smith, 2010). Ongoing sampling of

deep-sea communities continues to uncover new spe¬

cies, even in areas that are relatively well studied like

the NW Atlantic (Grassle and Maciolek, 1992). However,

the deep-sea is biologically nutrient-limited, and many

species appear to live in very low densities. So deep-sea

species may rely on strong dispersal mechanisms to find

sufficient habitat and thus have generally larger ranges

than shallow water species both in terms of depth range

and geographic range (Costello et al., 201 1). The primary

data for this pattern comes from fish rather than benthic

invertebrates, therefore it may not be valid to infer a

global generalization. Indeed, patterns in bathymetric

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THE NAUTILUS, Vol. 131, No. 1

ranges in the pelagic realm are very similar to latitudinal

ranges of terrestrial groups (Brown et ah, 1996). Deep-

sea benthic habitats are heterogeneous and represent

landscapes that vary on scales ol hundreds of kilometers

(Levin et ah, 2001), which is not dissimilar to the magni¬

tude ol some continents. As a result, how many deep-sea

species are endemic to the specific area where they

were discovered, or simply have only been found there

because ol poor sampling, remains highly debated.

Apart from this overall diversity on the undersea

mountains, valleys, and plains, there are oases that host

astonishing high-density biomass in chemoautotrophic-

based ecosystems. Geothermal energy is the foundation

for hydrocarbon “cold seeps and hydrothermal vents, or

direct nutrient input can come from organic falls (such

as whale carcasses and wood). All represent high-quality

energy input to the deep-sea ecosystem constrained at a

very small spatial scale (Gage and Tyler, 1992).

Food chains building on chemoautotrophic microbes

form a suite ol specialist animal species that is unique to

each type ol ecosystem. Specialist vent endemic species

cannot live in other deep-sea sites such as whale falls

(Wolff, 2005), and there is little overlap in vent and seep

fauna. There are some ecological similarities among these

“oases”, and some larger evolutionary radiations such

as hathvmodioline mussels or lepidopleuran chitons

include species that colonize different deep-sea hab¬

itats (Thubaut et ah, 2013; Sigwart, 2016), but each

species is restricted to its own specialism.

At hydrothermal vents, seawater circulating through

the seafloor is heated and enriched with reduced com¬

pounds; when the fluids emerge back into the main

ocean, minerals precipitate around the fluid flow, often

creating characteristic chimneys or “black smokers”.

Images of these habitats show the vertical walls of the

chimneys teaming with life (Figure 1 ), and the vent eco¬

systems are dominated by relatively few species occur¬

ring in very high biomass, comparable to the density of

life supported by tropical coral reefs (Van Dover, 2000).

The gastropods living in vent ecosystems include

a large number of endemic lineages (McArthur and

Tunnicliffe 199S), including unusual recently-derived adap¬

tations such as the “scaly-foot” gastropod ( Chn/somallon

squamiferum Chen et ah, 2015) in the Indian Ocean (Chen

et ah, 2015a). Each mollusk species lives in a “Goldilocks

zone” (not too hot and not too cold) with very narrowly

defined limits of temperature and ocean chemistry, some¬

where on the gradient where mineral-rich superheated vent

fluid emerges at over 300°C and is rapidly cooled by

surrounding seawater at around 2°C. Species’ varying

tolerances for temperature and acidic vent fluid create

patches or zones dominated by particular taxa, much like

the zonation in rocky intertidal shores (Van Dover, 2000).

Hydrothermal vents were first discovered in 1977

(Lonsdale, 1977; Van Dover, 2000). The identification of

these self-contained ecosystems at 2550 m depth on the

Galapagos Rift was a sea change for biology. Much of our

knowledge about vent systems in general, is based on

generalizations predicted from these earliest-discovered

and best-understood sites. Since then, other vent sites,

hosting different specialist communities, have been dis¬

covered in every ocean and more remain to be found

(Rogers et ah, 2012). Vents are known to occur at all

actively spreading ocean ridges, back-arc basins, and

some seamounts. Here we consider the impact of

the advance of knowledge about deep sea ecosystems

on our understanding of mollusean biodiversity and

its conservation.

HYDROTHERMAL VENTS, FAST AND SLOW

The tectonic geology of the seabed is different, in differ¬

ent ridge systems around the globe. There are at least

Figures 1-2. The Kairei Vent Field, Central Indian Ridge. 1. Overview of the Monju site in the Kairei Vent Field, the foreground

is covered by anemones, the spires of chimneys are covered by dense aggregations of vent shrimp (one seen swimming in

foreground). 2. Chrysomallon squamiferum from the Kairei Vent Field, shell length = 39.1 mm.

J.D. Sigwart et al., 2017

Page 45

1 1 distinct biogeographic provinces among vent systems

along the mid-ocean ridges and back-arc spreading cen¬

ters of the global seafloor (Rogers et ah, 2012). The

distribution of animals among these widely separated

habitats is largely explained by the local sea-floor spread¬

ing rates (Tunnicliffe and Fowler, 1996). Fast-spreading

centers such as East Pacific Rise (EPR) have rapidly

forming black smoker chimneys that are prone to col¬

lapse and re-grow on sub-decadal timescales (Shank

et ah, 1998); slow spreading centers, such as the South¬

west Indian Ridge, may have physical vent structures

and communities that are stable over multi-decadal or

even much longer timescales (Lalou et ah, 1990). Vent

fields that are close to each other, on a scale of hundreds

of kilometers apart, have similar but often non-identical

species assemblages (Van Dover, 2001) whereas vent

systems on different ocean ridges represent entirely

different faunas (Ramirez-Llodra et ah, 2007; Rogers

et ah, 2012).

The majority of detailed studies come from EPR and

the mid-Atlantic ridge, which are distinctly different

from all other global vent fields in terms of their fauna,

biogeography, dispersal potential, and spreading rates

of the underlying geology (Van Dover et ah 2002). The

first exploration of vent fields in the Indian Ocean

showed relatively minor differences in underlying geol¬

ogy compared predicted patterns, but dramatically dif¬

ferent fauna (Van Dover, 2001).

Despite these clear differences, the uniquely fast

turnover of the EPR fauna seems to be the basis of

generalizations about hydrothermal vent ecosystems.

Other vent systems, with slower turnover, are inevitably

more sensitive to and much slower to recover from

any disturbance.

Conservation of the deep sea, including hydrothermal

vents, must account for the modern understanding of

geographical variation in ecosystems. Hydrothermal

vents occur even at the slowest spreading portions of

global mid-ocean ridges such as the Southwest Indian

Ridge and the Arctic Ocean (Tivey, 2004; Pederson,

et ah, 2010). Slower spreading seems to correlate

with more stable faunal communities, low natural dis¬

turbance, and probably higher sensitivity and slower

recovery from disturbance (Van Dover, 2014); however,

these same slow-spreading centers may also generate

comparatively large mineral deposits (Tao et ah, 2014).

Thus the most sensitive areas are the primary target for

commercial exploitation. And the assessment of the

potential damage of that exploitation is inferred from a

dissimilar system.

Individual vent fields vary’ in scale but tend to be at

most a few kilometers across. Images of dense biomass

can be misleading, as the surrounding context of empty

ocean is never visible. Some iconic vent sites are actually

tiny; the Kairei Vent Field on the Central Indian Ridge,

where the scaly-foot gastropod was first discovered,

covers an area 80x30 m, less than half the size of a

football field (Van Dover, 2001). Contrast this to feasi¬

bility studies, which have shown that current demand

for rare earth minerals for only one gear’s global con¬

sumption requires extraction of 5 km- of seabed (Kato

et ah, 2013). That represents mining activity over more

than 2000 times the size of the entire Kairei Vent Field,

every year.

It is unclear whether the value of the minerals

extracted could ever offset the extreme cost and risk of

deploying mining equipment to the deep sea, and the

environmental damage caused to the seabed.

DEEP-SEA MINING

Tbe United Nations (1994a) Convention on the Law of

the Sea (UNCLOS) laid boundaries for the control of

coastal access and coastal resources. Territorial waters

of each nation extend only 12 nautical miles (22.2 km)

from the low-water mark of its coastline, and the Exclu¬

sive Economic Zone (EEZ) extends beyond that to a

further distance of up to 200 nautical miles (370.4 km).

Within this region (and some additional distance where

the continental shelf extends beyond the 200 nautical

miles limit), each country holds control of the seabed

and the pelagic realm for mining, fishing, and other

activities. Beyond that limit, the great majority of the

area and volume of the Earth’s oceans, are “interna¬

tional waters”, the high seas, mare liberum-, belonging

to no-one and everyone. All states have equal freedom

of passage, fishing, and access for research in interna¬

tional waters.

The legal control of the oceans is defined by distance

from land, not by depth. What constitutes “deep” sea is

not strictly defined, and the physical properties of sea¬

water at depth (solar penetration, temperature, oxygen,

current speeds) vary in different parts of the globe, but a

minimum of 1000 m is generally accepted as biologically

“deep” (Gage and Tyler, 1992). Coastal shells that are

familiar in commercial trade come from near shore —

even collectible species that are colloquially referred to

as "deep water” are almost all captured within the exclu¬

sive economic zone of the country of origin. For exam¬

ple, many species and forms of Zoila spp. from Australia

are sold as “deep water” cowries, but live mainly within

the limits of deep human diving, to a maximum depth of

perhaps 300 m (Lorenz and Hubert, 2002). Most people

think of Nautilus spp. as “deep-sea shells”, yet their

shells actually implode at depths of around 750-900 m

(Kanie and Hattori, 1983; Vermeij, 1993). The family

Pleurotomariidae or "slit shells” is famous as a group of

generally rare and collectible “deep-sea” gastropods, but

their bathymetric range only extends to a maximum just

shy of 1000 m (Harasewych, 2002).

We may think of the high seas as inaccessible, and not

available for commercial exploitation, apart from the

rather transient activities of shipping and fishing. The

seafloor of the “free seas” may seem both practically and

financially remote, and under the implicit protection of

the United Nations. In implementing the Convention on

the Law of the Sea (United Nations, 1994a), the United

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THE NAUTILUS, Vol. 131, No. 1

Nations (1994b) established the International Seabed

Authority (ISA) exactly to administer access to the floor

of the ocean beyond states’ jurisdiction (Jaeckel, 2015).

The text of the original UN resolution includes the state¬

ment that it was:

“Reaffirming; that the seabed and ocean floor . . . are

the common heritage of mankind. Mindful of the

importance of the Convention for the protection

and preservation of the marine environment and

of the growing concern for the global environ¬

ment . . .” (United Nations, 1994b: 3)

In July 2016, the ISA published a full working draft of

exploitation regulations to govern the active extraction

of minerals from mining the seabed in the high seas

(ISA 2016). Exploration for commercial deep-sea min¬

ing is already well underway. The first set of 15-year

licenses for mining exploration issued by the ISA to

governments anti commercial mining interests have

already expired. Exploration licenses were granted to

seven different groups from Europe, Russia, Korea,

China, Japan, and India, with contracts starting in

2001-2002, and all have applied for contract extensions.

The challenge for the ISA is to balance commercial

pressures with a mandate to manage conservation, in a

data limited environment and a largely untested legal

framework (Jaeckel, 2016).

The reality' of deep-sea mining, including heavy machin¬

ery deployed to the abyss, seems to stand in stark con¬

trast to the unexplored inaccessible mysteries of the

deep. But the technology is rapidly advancing, driven by

potential access to valuable rare minerals, and interna¬

tional competition for first access to a new commercial

frontier (Hoagland et ah, 2010; Aldhous, 201 1). The key

targets of seabed exploitation are polymetallic nodules,

polymetallic sulfides, and cobalt-rich ferromanganese

crusts. Sulfides, rare earth minerals, and rare metals,

including cobalt, are found in high densities at sites of

geological spreading activity, such as hydrothermal vents

(Tao et ah, 2014; Van Dover, 2014).

The vivid images of dense communities and biomass at

hydrothermal vents, in an ecosystem with no sunlight,

are now a familiar part of deep-sea biology. The geolog¬

ical setting of vents creates habitat, small oases in the

deep sea dependent on geothermal energy, but also

exploitable concentrations of mineral deposits. Thus,

vent areas globally became focal points for both con¬

servation concerns and commercial exploitation. This

conflict has been dismissed in many studies, based on

misunderstanding of the diversity of vent geology and

vent biota.

OUT OF SIGHT, BUT NOT OUT OF MIND

There are important reasons that prevent deep-sea

mollusks from direct commercial exploitation for the

shell collecting trade. Publicly funded scientific expe¬

ditions are currently the only mechanism for collecting

these shells in most localities. To ensure the protec¬

tion, preservation, and inclusive scientific access to

this precious material, they belong in permanent, pub¬

licly available museum collections, not in the control

of individual researchers or private citizens. Public

education about these animals is also crucial to their

future survival. A disconnect between scientists and

mollusk enthusiasts may he to the detriment of conser-

vation efforts.

We consider the scaly-foot gastropod, Chrysomallon

squamifemm (Chen et ah, 2015a: Figure 2), as a case

study of an animal that is popular and well-known, but

that lacks protection or detailed study in its own hydro-

thermal vent habitat. The scaly-foot gastropod is an

iconic member of the Indian Ocean hydrothermal vent

fauna, known for the mineralized scales that cover the

outer surface of its foot (Chen et al., 2015b). This species

has been reported from only three sites since its discov¬

ery in 2000. Its total habitat covers less than 0.02 km2 or

less than one-fifth of a football field in total range, spread

over an area of nearly 1,000,000 km2 (925,347 kin2)

(Figure 3).

Among the three sites where the scaly-foot has been

reported, two are located in Area’s Beyond National

Jurisdiction (ABNJ) and therefore fall under the legal

mandate of the ISA. The Solitaire Vent Field occupies

an area of 50x50 m and is within the EEZ of Mauritius

(Nakamura et al., 2012). The Kairei Vent Field is of very

similar size, at around 30x80 m (Van Dover et al., 2001),

but 773 km south of Solitaire, the entire area of Kairei

Vent Field is under an active mining exploration license

granted to Germany (2015-2030) by the ISA. The third,

southernmost reported population is located 2563 km to

the southwest, at Longqi Vent Field. There, the main

vent field spans 100x150 m (Tao et al., 2014), and this

and the surrounding areas are under a mining explora¬

tion license granted to China (2011-2026). The conser¬

vation status of this species has not yet been assessed by

the IUCN, although a population genetic study examining

the connectivity among the three populations revealed

poor connectivity between Longqi and the other two pop¬

ulations, implying dispersal barrier exist across the two

ridges (Chen et al., 2015c). There are no conservation

measures in place, and none have yet been proposed,

for any of these sites.

Each hydrothermal vent site, especially those in the

remote Indian Ocean, are observed on average less

than once a year by the collective global endeavor of

scientists, and independent monitoring of any commer¬

cial activity in such sites is nearly impossible. There is a

small island in the River Thames, UK, designated as a

nature reserve to protect terrestrial snails and other

wildlife (Burns et al., 2013). At 9 acres (0.035 km2),

Isleworth Ait is almost twice the area of the entire

known habitat for Chrysomallon squamifenim , and

this island is not the only reserve for the two-lipped

door snail Alinda biplicata (Montagu, 1803). Addi¬

tional protection for deep-sea biota would seem to

be warranted.

J.D. Sigwart et al., 2017

Page 47

Figure 3. Infographic depicting the relative scale of hydrothermal vent sites. Top left, the area of Kairei Vent Field on the Central

Indian Ridge is shown as the blue box relative to a sports field conforming to regulations of Federation Internationale de Football

Association (FIFA), 105x70 m. Top right, the sum of all Indian Ocean hydrothermal vent fields, represented to scale in green playing

fields, against an 1 km2 black square. This area was calculated based on a count of 37 reported Indian Ocean sites of vent activity

according to the InterRidge international database, and an arithmetic average size of 7225 m“ per vent field, based on the four welb

mapped confirmed active sites (Edmond, Kairei, Solitaire, Longqi). The island of Mauritius is shown with approximately 1-km grid

squares. At bottom left, the map of the Indian Ocean compares the location of Mauritius and the three vent sites where the scaly-foot

gastropod, Chrysomallon squamiferum, has been found (Solitaire, Kairei in blue, and Longqi; boxes not to scale).

There are more than 712 animal species described

from hydrothermal vents, in only 40 years since the first

dramatic discovery of these ecosystems (Wolff, 2005).

Among these are more than 250 mollusk species and that

number is continuously increasing. Study of hydrother¬

mal vents changed thinking about the limits of life on

earth, expanding to a world without solar energy (Van

Dover, 2000). This has expanded scientific knowledge

but also enriched the understanding of our planet for

everyone. Scientists and citizens alike have a role to

voice concern over potentially permanent damage to

the deep oceans.

ACKNOWLEDGM ENTS

The authors thank Jose H. Leal, Smoky and Stephanie

Payson, and Dorrie Hipschman for the opportunity to

present this work at the “Mollusks in Peril’' 2016 Forum at

the Bailey- Matthews National Shell Museum in May 2016.

Comments from two anonymous reviewers improved an

earlier version of this manuscript. We also thank Ken Takai

(|AMSTEC) for inviting ns on-board the R/V Yokosuka

cruise YK16-E02 to explore tire hydrothermal vents of

Indian Ocean, and for allowing us to use an image taken

during that cruise as Figure 1 herein.

Page 48

THE NAUTILUS, Vol. 131, No. 1

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mollusks in peril

2016 forum

presented by

gj BAILEY- MATTHEWS

^ NATIONAL SHELL MUSEUM

End of the Mollusks in Peril 2016 Forum Section

THE NAUTILUS 131 ( 1 ):51-66, 2017

Page 51

Taxonomic reexamination of three vesicomyid species (Bivalvia)

from the middle Miocene Bessho Formation in Nagano

Prefecture, central Japan, with notes on vesicomyid diversity

Yusuke Miyajima

Department of Geology and Mineralogy

Graduate School of Science, Kyoto University

Oiwakecho, Kitashirakawa, Sakyo-ku,

Kyoto 606-8502, JAPAN

[email protected]

Takami Nobuhara

Faculty of Education, Shizuoka University

836, Oya, Suruga-ku

Shizuoka 422-8529, JAPAN

Hakuichi Koike

Shinshushinmachi Fossil Museum

88-3, Kamijo, Shinshushinmachi

Nagano 381-2404, JAPAN

ABSTRACT

The middle Miocene Bessho Formation in central Japan

consists of siltstone deposited on the slope of a back-arc basin,

and contains cold-seep carbonate bodies of various sizes.

We describe four vesicomyid species from this formation, one

of them new, Pliocardia ? tanakai new species, one in open

nomenclature, Adulomtja sp. 1, and two previously reported

species, Adulomija uchimuraensis Kuroda, 1931 and Calyptogena

akanudaemis Tanaka, 1959, the latter here reassigned to

the genus Adulomija . The relative abundances of the four

vesicomyid species are different among fossil localities, appar-

endy related to size, lithology, and the carbon isotopic signature

of the carbonate bodies. First, large carbonate mounds com¬

posed of micrite and calcite veins, with 51 ’C values of —40 to

— 36%o vs. PDB, are dominated by A. uchimuraensis , with

A. akanudaensis and Pliocardia? tanakai new species being

minor constituents. Second, siltstone containing em-sized car¬

bonate concretions with 51 ’C values as low as — 35%o contains

only rare and scattered specimens o { Adulomtja sp. 1. Third, at

a carbonate body, ~1 m in diameter and composed mainly of

micrite with 51 3C values of —29.8 to -F 1 0.5%o, A. akanudaensis

and A. uchimuraensis are about equally abundant. These dis¬

tribution patterns suggest that the vesicomyid species diversity

in the Bessho Formation might have been related to variations

in the physico-chemical characteristics of the seep environ¬

ment, such as fluid flux rates and/or seep longevity.

Additional Keywords: Pliocardia, new species, Adulomija,

Vesicomyidae, middle Miocene, cold seeps

INTRODUCTION

Vesicomyid bivalves first appeared at the middle Eocene

cold-seep sites in North Pacific, and they are now domi¬

nant animals in various deep-sea reducing environments

such as cold seeps, hydrothermal vents, and whale falls

all over the world (Amano and Kiel, 2007; Taylor and

Glover, 2010; Krylova and Sahling, 2010). The family

Vesicomyidae is one of the most species-rich families

among ehemosynthesis-based animals, with more than

100 species described so far (Decker et ah, 2012). A

recent molecular phylogenetic analysis of the vesieomyids

by Decker et al. (2012) suggested recurrent events of

“stepwise speeiation” from shallow to deep waters in

different ocean basins, which is consistent with bathy¬

metric segregation among the extant genera and species

(Fujikura et ah, 2000; Cosel and Oln, 2009; Krylova

and Sahling, 2010). For more discussion on vesicomyid

species diversity we should also pay attention to

co-occurrences of two or more species from the same

area, both in modern (e.g., Callender and Powell, 1992;

Barry et ah, 1997; Kojima and Ohta, 1997; Krylova and

Janssen, 2006; Fujikura et ah, 2008) and ancient seep

sites (Tanaka, 1959; Amano et ah, 2010; Kiel, 2010; Kiel

and Amano, 2010; Amano and Kiel, 2012).

The middle Miocene Bessho Formation in Nagano

Prefecture, central Japan, hosts cold-seep carbonate

bodies of various sizes, some of which yield two or more

vesicomyid species (Koike and Miyajima, 2016). The

large seep carbonate bodies at Akanuda and Anazawa

have been reported to yield two vesicomyid species,

Adulomya uchimuraensis Kuroda, 1931, and Calyptogena

akanudaensis Tanaka, 1959 (Tanaka, 1959; Kanno et ah,

1998). Adulomija uchimuraensis has been studied and

revised by Kanno et ah (1998) and Amano and Kiel

(2011), but C. akanudaensis was beyond the scope of

these studies and its generic assignment was postponed,

because its internal characters were unknown.

This paper focuses on taxonomical reexamination on

vesicomyid species from the Bessho Formation. We reas¬

sign Calyptogena akanudaensis to the genus Adulomya

Kuroda, 1931, on the basis of its internal shell characters

recognized in type materials and our newly collected

fossil specimens. We also newly describe Pliocardia?

tanakai new species and report another species, Adulomya

sp. 1 , in open nomenclature. Habitat preferences of the four

species are discussed based on their relative abundance,

Page 52

THE NAUTILUS, Vol. 131, No. 1

mode of occurrences, and the petrographic and geo¬

chemical characteristics ol the hosting seep carbonates.

MATERIALS AND METHODS

The Bessho Formation is mainly composed of dark-gray

siltstone deposited at a back-arc basin after the opening

of the Japan Sea (Harayama, 2006). The examined

vesicomvid fossils are from three localities in the north¬

ern part of Matsumoto City, i.e., Akanuda and Anazawa

(Loe. 1), Sorimachi (Loc. 2), and Tonohara (Loc. 3), as

shown in Figure 1. Kato et al. (2011) estimated the

sedimentary environment of the Bessho Formation to

be upper- to upper middle-bathyal depths under warm

current, based on a benthic foraminiferal assemblage

from Loc. I and other fossil occurrences (Kosaka

and Taguchi, 1983; Noda et ah, 1986; Itoigawa and

Yanagisawa, 2002). Kato et al. (201 1) assigned the plank¬

tonic foraminiferal and calcareous nannofossil assem¬

blages from Loc. 1 to the PF2/PF3 zones of Maiya

(1978) and the CN5a zone of Okada and Burkry (1980),

corresponding to an absolute age of 13.6 to 13.1 Ma,

according to Saito (1999).

We reexamined vesicomyid fossil specimens in the

collection of Kunio Tanaka (Emeritus Professor of

Shinshu University, Japan) from seep carbonate bodies

at Akanuda and Tonohara (Locs. 1 and 3), which are

deposited in the Shinshushinmachi Fossil Museum

(SFMKT-00144, 00389, 00398, 00399, 00401-00407, and

07227-07230). In addition, abundant vesicomyid fossil

specimens collected by us from the three localities were

also examined. The specimens were carefully cleaned

cJdc

138'E.

Legend

□ Ogawa Formation

□ Aoki Formation

S Bessho Formation

Uchimura Formation

/ Faults

XX Syn- & Anticline axes

• Fossil locality

Matsumoto

Figure 1. The geological map of the northern area of

Matsumoto City, Nagano Prefecture (modified from Seki, 1983;

Yamada et al., 1989; Nakano et al., 1998; Harayama et al., 2009)

showing the localities of the vesicomyid fossils described herein.

1; Anazawa and Akanuda limestones. 2: Sorimachi. 3: Tonohara.

using an air scribe and needles to expose hinge characters,

measured to the nearest 0.1 mm using a caliper, and

photographed with ammonium chloride coating. All spec¬

imens are deposited in the Shinshushinmachi Fossil

Museum (SFM) and the Department of Geology and

Mineralogy, Kyoto University, Japan (KUG).

We analyzed carbon stable isotopic compositions of the

carbonates from localities 2 and 3, in order to examine

whether or not they were related to methane seepage.

Powdered samples, taken from cut slabs using a micro¬

drill, were reacted with 100% orthophosphoric acid in

vacuum at 90 °C for 1000 s, and analyzed in a mass

spectrometer IsoPrime 100 (Isoprime) at the Department

of Geology and Mineralogy, Kyoto University. Isotope

values are expressed as a per-mil difference between the

sample and the PDB standard in delta notation. External

precision for the standard material was better than 0.1%o.

LITHOLOGY AND MODE OF

FOSSIL OCCURRENCE

Seep carbonate size, lithology, and mode of fossil occur¬

rence differ among the studied localities. At Akanuda and

Anazawa |Loc. 1), large-sized seep-carbonate mounds, up

to 20 m in diameter, are intercalated within the dark-gray

massive siltstone (Figure 2). The carbonate mounds

consist of muddy micrite with sparitic veins and veinlets,

both showing low 81 !C values (—40 to — 36%o vs. PDB;

Sato et al., 1993) originating from the anaerobic oxidation

of methane (Peekmann and Thiel, 2004). These seep car¬

bonates yield abundant molluscan fossils dominated by a

large and elongate vesicomyid, Adulomya uchimuraensis ,

with patchy clusters of a bathymodiolin mussel,

“Bathymodiolus” akanudaensis (Tanaka, 1959) (Tanaka,

1959; Kanno et al., 1998; Nobuhara et al., 2008;

Nobuhara, 2010). In addition, the fossil fauna of the seep

carbonates at this locality is characterized by a high

species diversity, including bivalves Conchocele bisecta

(Conrad, 1849), Lucinoma sp., and Megathracia sp., and

gastropods Provanna sp., Margarites sp., Comitas sp., and

Trophonopsjs sp. The vesicomyid A. uchimuraensis

and "B.' akanudaensis often form shell clusters composed

of conjoined valves, indicating in-situ burial of the colo¬

nies (Figure 3). Tanaka (1959) described Calyptogena

akanudaensis from Akanuda, but we failed to collect new

specimens of this species from this locality, suggesting

that it is a rare species. Tanaka (1959) also reported the

bivalves Paphia sp. and Liocyma cf. terrera from

Akanuda, both of which are here redescribed as a new

vesicomyid species, Pliocardia? tanakai new species. We

found seven additional specimens of this species, three

of which were collected from the marginal part of the

carbonate mound at Anazawa.

At Sorimachi (Loc. 2), located about 1.3 to 1 .5 km west

of Loc. 1, dark-gray siltstone containing small carbonate

concretions, several centimeters in diameter, is exposed

on a riverside cliff of the Hofukuji River (Figure 4). The

carbonate concretions show §13C values as low as — 35%o,

Y. Mivajima et al., 2017

Page 53

Figures 2-7. Study outcrops. 2. Large seep carbonate body at Anazawa, Loc. 1 . Seale bar - 1 m. 3. Cluster of articulated valves ol

Adulomua uchimuraensis Kuroda in the carbonate body at Loc. 1. Scale Bar =0.1 m. 4. Siltstone containing abundant small

carbonate concretions at Sorimaehi, Loc. 2. Scale bar = 1 in. 5. Single articulated valves of Adulomija sp. 1 contained in the siltstone

at Loc. 2. White arrow points a carbonate concretion. Scale bar = 10 mm. 6. Carbonate block at Tonohara, Loc. 3. Square indicates

three fossils of A. akanudaensis enlarged in 7. Scale bar = 0.2 m. 7. Cluster of three articulated valves of A. akanudaensis (Tanaka)

contained in the carbonate block at Loc. 3. White arrows indicate each fossil and its anterior direction. Note that all valves are

arranged in parallel with their anterior sides in similar directions. Scale bar = 10 mm.

suggesting methane seepage at this site (details will be

reported elsewhere). Mostly conjoined shells of small

and elongated vesicomyid fossils are scattered through¬

out the siltstone, with their commissure planes parallel to

the bedding plane (Figure 5). The species composition

at Loc. 2 is monotonous and consists mainly of this

vesicomyid, with rare lucinid and solemyid bivalves.

Although the vesicomyid fossils from this locality were

once identified as Adulomija uchimuraensis by Tanaka

(1960) and Seki (1983), we show that they are distin¬

guishable from A. uchimuraensis and report them in

open nomenclature, as Adulomya sp. 1.

Page 54

THE NAUTILUS, Vol. 131, No. 1

At Tonohara (Loc. 3), a carbonate body of ~1.1 m

diameter is exposed on a slope (Figure 6). This carbonate

body is entirely mieritic, lacks sparitic cement, and has

51 'C values ranging from -29.8 to +10.5%o. Those parts

of the carbonate body having positive 51 5C values could

have originated from the 1 ’C-enriehed C02 pool in the

methanogenesis zone (Irwin et ah, 1977), whereas those

parts showing negative and low 51 'C values could have

formed via the anaerobic oxidation of methane, suggest¬

ing that this locality was affected by methane seepage.

This carbonate body contains Adulomya uchimuraensis ,

“Calyptogena” akanudaensis , Conchocele sp., and gastro¬

pod fossils. The species composition is similar to that

of the large carbonate mounds at Akanuda and Anazawa

(Loc. 1), but it differs from the latter in 1) “C.”

akanudaensis and A. uchimuraensis being about equally

abundant, and 2) having a lower species diversity lacking

Bathymodiolus , Pliocardia , and Provanna. Most bivalve

fossils are conjoined and often found in in-situ burial

mode, in which all valves are arranged in parallel with

their anterior sides in similar directions (Figure 7).

SYSTEMATIC PALEONTOLOGY

Family Vesicomyidae Dali and Simpson, 1901

Subfamily Pliocardiinae Woodring, 1925

Genus Pliocardia Woodring, 1925

Type Species: Anomalocardia howdeniana Dali, 1903

from the upper Pliocene Bowden Formation in Jamaica

(original designation).

Remarks: Krylova and Janssen (2006) redefined the

genus Pliocardia as small- to medium-sized elliptical

vesicomyid characterized by a shallow radial depression

from umbo to postero-ventral margin, a deep lunular

incision, a shallow pallial sinus, and a stout ventral tooth

(1) overlying the subumbonal cardinals (3a, 3b) in the

right valve. Pliocardia is similar to Vesicomya in its

small shell size, clearly incised lunule, and dentition

(Woodring, 1925), but differs from the latter by having

thicker shells and a much thicker posterior cardinal tooth

(Amano and Kiel, 2007). Pliocardia is also similar to

Archivesica Dali, 1908 in dentition, but distinguished

from the latter by having a much smaller shell and an

escutcheon, and lacking a subumbonal pit (Amano and

Kiel, 2007, 2010; Krylova et ah, 2014).

Recently, Martin and Goffredi (2012) acknowledged a

need for a taxonomic revision of Pliocardia. They newly

described “ Pliocardia ” krylovata from the Costa Rica

Margin based on molecular evidence. “ Pliocardia ”

krylovata has a thick shell, a shallow postero-ventral

depression, a shallow lunular incision, a shallow but

complex pallial sinus, and a remarkably deep escutcheon.

The latter two characters have not yet been recognized in

Pliocardia (sensu stricto).

Pliocardia? tanakai new species

(Figures 8-23)

Liocyma cf. terrera (Yokoyama). — Tanaka, 1959: 121-122,

pi. 3, figs. 21-22.

Paphia sp. Tanaka, 1959: 122, pi. 3, fig. 23.

Diagnosis: Small-sized ovate vesicomyid with pointed

posterior end in adult, well-defined lunular incision, ven¬

tral cardinal tooth (1) thick and anterior cardinal tooth

(3a) very short in right valve hinge, anterior cardinal tooth

(2a) thin and middle cardinal tooth (2b) knob-shaped,

both connected at nearly right angle in their proximal

parts just below umbo in left valve hinge, a blunt ridge

from umbo to postero-ventral corner on internal surface

but no radial depression on external surface which corre¬

sponds to the internal blunt ridge, pallial sinus lacking.

Description: Shell thin, small in size (up to 28.4 mm

in length), ovate in outline (height/length = 0.57-0.78),

more rounded in juvenile (length < 16 mm), equivalve

and inequilateral, moderately inflated (width/length =

0.28-0.55), ornamented with fine commarginal growth

lines. Antero-dorsal margin slightly concave, continuing

to rounded and slightly convex anterior margin; postero-

dorsal margin nearly straight, obtusely angulate at tran¬

sition to posterior margin; posterior margin rounded in

juvenile but more pointed with growth; ventral margin

broadly arcuate. Beak prominent, prosogyrate and located

at 26-38% of shell length from anterior end. Lunule well

defined by distinct lunular incision. Escutcheon narrow

and shallowly depressed. Right valve hinge: ventral cardi¬

nal tooth (1) moderately thick, subparallel to antero-dorsal

shell margin, overlain by anterior cardinal tooth (3a) in its

posterior end; anterior cardinal (3a) very short, parallel

to shell margin; entire shape of posterior cardinal (3b)

unclear due to recrvstallization of the shell. Left valve

hinge: anterior cardinal (2a) thin, parallel to antero-dorsal

shell margin; middle cardinal (2b) short and knob-shaped,

situated just below umbo, connected with anterior cardi¬

nal (2a) at nearly right angle in their proximal parts; pos¬

terior cardinal (4b) slightly thinner but as long as anterior

cardinal (2a), subparallel to postero-dorsal shell margin,

detached from other cardinals (2a and 2b). Anterior

adductor muscle scar ovate with rather straight and deeply

impressed posterior margin. Posterior adductor muscle

scar ovate with deeply impressed anterior margin forming

a blunt inner ridge running from beak. Pallial line entire,

starting at postero-ventral corner of anterior adductor

scar and connecting to antero-ventral corner of posterior

adductor scar without pallial sinus.

Measurements: See Table 1 .

Holotype: Right valve preserving its dentition and

adductor muscle scars with pallial line on internal mold,

SFMCM-0182 (Figures 11 and 12).

Paratypes: One left valve with its dentition preserved,

SFMCM-0178 (Figures 8-10); four closed valves partly

Y. Miyajima et al., 2017

Page 55

Figures 8-23. Pliocardia ? tanakai new species. All specimens are from Loe. 1. 8-10. Lateral (8) and dorsal (9) views, and hinge

(10) ol left valve; Paratype, SFMCM-0178. White arrow shows lunular incision. 11-12. Right valve hinge (11) and inner mold of

right valve (12); aas, anterior adductor muscle scar; Holotvpe, SFMCM-0182. White arrow shows lack of pallia] sinus. 13-15. Dorsal

(13), left lateral (14) and right lateral (15) views; aas, anterior adductor muscle scar; pas, posterior adductor muscle scar; Paratype,

SFMCM-0180. White arrows show lunular incision (13) and lack of pallia! sinus (14). 16. Right lateral view with inner mold in part;

Paratype, SFMCM-0181. 17-18. Left lateral view (17) and right lateral view with inner mold in part (18); Paratype, SFMCM-0183.

19-21. Dorsal view (19), left lateral (20) and right lateral (21) views of inner mold; aas, anterior adductor muscle scar; pas, posterior

adductor muscle scar; Paratype, SFMCM-0179. White arrow shows lack of pallia! sinus. 22-23. Right lateral (22) and left lateral

(23) views of inner mold; SFMKT-00399. Scale bar = 10 mm (for all figures).

exhibiting internal molds with adductor scars and pallia!

lines, SFMCM-0180 (Figures 13-15), 0181 (Figure 16),

0183 (Figures 17 and 18), 0179 (Figures 19-21):

Other Examined Material: One inner mold of both

valves, SFMCM-0184; three conjoined valves from

Loc. 1, which were once described by Tanaka (1959) as

Liocyma ef. terrera (No. 520 in Tanaka, 1959, pi. Ill,

figs. 21 and 22), registered now as SFMKT-00398, and

Paphia sp. (No. 521 in Tanaka, 1959, pi. Ill, fig. 23),

registered now as SFMKT-00399.

Type Locality: Akanuda and Ai lazawa, Matsumoto

City, Nagano Prefecture, central Japan (Loc. 1 in Figure 1).

Distribution: Only from the type locality, middle

Miocene Bessho Formation in Nagano Prefecture,

central Japan.

Etymology: Named after the Emeritus Professor

Kunio Tanaka, who made great contributions to the geol¬

ogy and paleontology of Nagano Prefecture.

Remarks: The present species is tentatively assigned

to the genus Pliocardia because of its ovate shell outline,

a right valve hinge having stout ventral cardinal (1) and

arched subumbonal cardinals (very short 3a and 3b), and

a distinct lunular incision, which are the diagnostic char¬

acters of the genus Pliocardia as redefined by Krylova

and Janssen (2006). However, this species lacks the

following two diagnostic characters: 1) a shallow pallial

sinus and 2) a radial depression on the external shell

surface running from the umbo to the postero-ventral

margin. Considering that the genus Pliocardia is taxo-

nomicallv uncertain at present as mentioned by Martin

and Goffredi (2012), we avoid at this point erection of a

new genus for this species.

This species is also similar to the species of

Waisiuconcha Beets, 1942, in its ovate or subcircular

shell outline, strong ventral cardinal (1) and arched

subumbonal cardinals (3a and 3b) in the right valve

hinge, well-defined lunular incision, and lacking of a

pallial sinus (Cosel and Salas, 2001). Waisiuconcha has,

however, a pallial line distant from the ventral margin,

while the present species has a pallial line close to the

ventral margin. Moreover, Waisiuconcha also lacks a

radial depression or an inner ridge on the shell surface.

Pliocardia? tanakai new species resembles the type

species of the genus Austrogena Krylova, Sellanes,

Valdes, and D'Llia, 2014, which was recently described

from the Chilean margin, in the presence of a lunule and

an escutcheon, its hinge dentitions of both valves, and

the absence of a pallial sinus. The genus Austrogena ,

however, has an oval to more rectangular shell and a less

impressed lunular incision than P.? tanakai. Moreover,

the hinge plate of adult Austrogena is characterized

by the presence of a subumbonal pit, which is absent in

P? tanakai. Austrogena is known only from the south¬

eastern Pacific at present (Krylova et al., 2014).

The genus Notocahjptogena Amano, Saether, Little,

and Campbell, 2014 also has a radial internal ridge sim¬

ilarly to Pliocardia? tanakai. However, Notocahjptogena

can be clearly distinguished from the present species by

its larger, elongate shell, a longer anterior cardinal tooth

(3a) in the right valve, and lacking a lunule.

Pliocardia? tanakai is the second Japanese fossil spe¬

cies assignable to this genus. Pliocardia kawadai (Aoki,

1954) has been known as the only Japanese fossil species

of this genus, and it has been reported from the lower to

middle Miocene seep and whale-fall sites in the central

to northern Japan (Amano and Kiel, 2012).

Comparisons: Pliocardia? tanakai new species can

be clearly distinguished from the other two Japanese

Pliocardia species, i.e., P. kawadai from the lower to

middle Miocene and the lixing species P. crenulomarginata

(Okutani, Kojima and Iwasald, 2002), by having a smaller

and lower shell (Figure 24) and by lacking a pallial sinus

and a distinct radial depression from the beak to the

postero-ventral corner on the external shell surface.

Pliocardia? tanakai resembles Pliocardia? sp. from the

upper Oligocene part of the Lincoln Creek Lormation in

western Washington State, USA (Amano and Kiel, 2007,

2012) in shell size and outline, but differs from it

in lacking a depressed area running from the beak to

the posterior corner on the external shell surface and

in having a weaker anterior cardinal tooth (3a) in the

right valve.

Amano and Kiel (2012) suggested that some of the

Paleogene vesicomyid species from the North Pacific

realm which were previously assigned to Archivesica,

including the oldest known vesicomyid '‘Archivesica'' ef.

tschudi (Olsson, 1931) from the upper middle Eocene

Humptulips Lormation in western Washington, USA,

may belong to Pliocardia. Pliocardia? tanakai resembles

“A”, cf. tschudi illustrated in Amano and Kiel (2007) in

having an ovate shell outline, an inner ridge just before

the posterior adductor muscle scar, and no pallial sinus,

but is distinct from the latter by a more posteriorly situ¬

ated beak, a non-undulated anterior cardinal tooth (2a),

and lacking of a subumbonal pit. P? tanakai is also

similar to Vesicomya aff. tschudi Olsson, 1931 reported

Y. Miyajima et al., 2017

Page 57

40,

35

30

?25

E

~ 20 \

D)

15

10-1

5

0

Pliocardia ? tanakai

•e- P. kawadai

-a- P. crenulomarginata

□ "Vesicomya" kaikoae

/S

tv

Os'*

(&/-

'O

/A

H = 0.646 L + 2.853

R2 = 0.988

R2 = 0.939

H = 0.551 L + 2.576 R2 = 0.921

0 10 20 30 40

Length (mm)

50

Figure 24. Relationships between shell length and height

with growth of Pliocardia ? tanakai new species, P. kawadai

(Aoki), P. crenulomarginata (Okutani, Kojima and Iwasald),

and “Vesicomya” kaikoae Okutani, Fujikura and Kojima. Mea¬

surements of P. kawadai are from Kamada (1962) and Amano

et al. (2001), those of P. crenulomarginata are from Krylova and

Janssen (2006), and those of “V”. kaikoae are from Okutani

et al. (2000).

by Squires and Gring (1996) from the upper Eocene

Wagonwheel Formation in California, USA, in its shell

size and shape. Although the specimens of Squires and

Gring (1996) did not show the hinge characters and

seems to he somewhat deformed, they are clearly distin¬

guishable from P.? tanakai by a truncated posterior end.

Pliocardia ? tanakai also resembles Pliocardia? sp.

from the lower to middle Miocene B exhaven Limestone,

New Zealand (Amano et al., 2014) in its shell outline

with a subtruncated posterior margin, a Iunular incision,

and a blunt ridge running from the beak to the postero-

ventral corner, but differs from the latter species in lack¬

ing a pallia] sinus. Moreover, the posterior cardinal tooth

(3b) of P.? tanakai is not as strong as that of Pliocardia?

sp. from the Bexhaven Limestone.

Some specimens of Calyptogena pacifica Dali, 1891

from the upper Miocene in Japan (Amano and Jenkins,

2011) have an ovate shell outline like Pliocardia?

tanakai. Calyptogena pacifica also has an escutcheon

and lacks a pallial sinus, but can be distinguished from

P.? tanakai by having a less inflated shell and lacking

a lunule.

Pliocardia? tanakai resembles the Recent “Vesicomya”

kaikoae Okutani, Fujikura and Kojima, 2000 in shell size

and outline (Figure 24), the presence of a Iunular inci¬

sion, and the right valve dentition having a ventral tooth

(1) overlaid by arched cardinals (3a and 3b). But

“ Vesicomya ” kaikoae has a pallial line with a shallow

embayment which is absent in P.? tanakai. Recently,

molecular phylogenetic analyses revealed that “V”.

kaikoae is well separated from the other vesicomyid spe¬

cies including Pliocardia species (Kojima et al., 2004;

Krylova and Sahling, 2010; Decker et ah, 2012).

Genus Adulomya Kuroda, 1931

Type Species: Adulomya uchimuraensis Kuroda, 1931

from the middle Miocene Bessho Formation in central

Honshu, Japan (monotypy).

Remarks: The genus Adulomya was redefined by

Amano and Kiel (2007) and characterized by its elongate

shell, two radiating cardinal teeth in the right valve

hinge, and lacking of a pallial sinus except for A. chitanii

Kanehara, 1937 (Amano and Kiel, 2011). Adulomya

first appeared in the eastern Pacific in late Eocene

age (Amano and Kiel, 2007) and invaded into Japan in

the early Miocene (Amano and Kiel, 2011). Japanese

Adulomya showed its high species diversity during early

to middle Miocene in lower sublittoral to middle bathyal

depths, but declined with replacement by other

vesicomyid genera such as Archivesica and Calyptogena

since the late Miocene (Amano and Kiel, 201 1).

Adulomya akanudaensis (Tanaka, 1959)

new combination

(Figures 25-44)

Calyptogena akanudaensis Tanaka, 1959: 119-120, pi. 2,

figs. 1-9; Amano and Kiel, 2011: 84, figs. 27-29.

Redescription: Shell thin, moderate in size (up to

71.1 mm long), elongated elliptical in shape (height/

length = 0.39-0.68), equivalve and inequilateral, slightly

to moderately inflated (width/length = 0.24-0.40), sculp¬

tured by fine commarginal growth lines with wider inter¬

spaces in posterior part. Antero-dorsal margin nearly

straight to slightly concave, graduating to rounded or

slightly protruded anterior margin; postero-dorsal mar¬

gin nearly straight and parallel to ventral margin or

slightly convex, continuing to rounded posterior margin;

ventral margin straight, broadly arcuate in juvenile

(length < 27 mm), or slightly concave at its central part

in some specimens. Beak low, prosogyrate, and situated

at 16-40% of shell length from anterior margin. Lunule

and escutcheon absent. Right valve hinge: anterior car¬

dinal tooth (3a) reduced; central cardinal tooth (1) small,

triangular, situated below umbo, with hollow space

between its dorsal end and umbo; posterior cardinal

tooth (3b) moderately thick, bifid, subparallel to postero-

dorsal shell margin, detached from central cardinal tooth

(1). Left valve hinge: anterior cardinal tooth (2a) thick,

oblique anteriorly, connecting with central cardinal tooth

(2b) in their proximal parts at acute angle; central cardi¬

nal tooth (2b) stout, situated just below umbo, tapered to

proximal part, nearly perpendicular to hinge base; poste¬

rior cardinal tooth (4b) thin, weak, oblique posteriorly,

connecting with central cardinal tooth (2b) as with

Page 58

THE NAUTILUS, Vol. 131, No. 1

Figures 25-44. Adutomija akanudaensis (Tanaka). Specimens of Figures 25-35 and 39-41 are from Loc. 1 (type locality) and

those of Figures 36-38 and 42 — 14 are from Loc. 3. 25-28. Left lateral view (25), dorsal view (26), and right lateral view of inner

mold (27), and left valve hinge (28); Neotype, SFMKT-00404. 29. Left lateral view with inner mold; Paratype, SFMKT-00401.

30-31. Right lateral view of a small specimen, SFMKT-00405-1 (paratype), attached on a large specimen, SFMKT-00405-2 (30), and

dorsal view of a large specimen, SFMKT-00405-2 (31). 32. Left lateral view with inner mold; Paratype, SFMKT-00406. White arrow

shows inner rib. 33-35. Left lateral (33), dorsal (34), and right lateral (35) views; Paratype, SFMKT-00403. 36-38. Right lateral

view (36), left lateral view of inner mold (37), and right valve hinge (38); pas, posterior adductor muscle scar; SFMCM-0191. White

arrow shows lack of pallia] sinus. 39-41. Left lateral view of inner mold (39), dorsal view (40), and right lateral view of inner mold

(41); Paratype, SFMKT-00402. 42. Right lateral view of inner mold; aas, anterior adductor muscle scar; pas, posterior adductor

muscle scar; SFMCM-0185. White arrow shows inner ridge. 43. Right lateral view; SFMCM-0189. 44. Right lateral view; SFMCM-0188.

Scale bars = 10 mm (for all figures).

Y. Mivajima et al., 2017

Page 59

anterior cardinal tooth (2a). Anterior adductor muscle

scar well impressed and ovate, with a distinct inner rib

running from beak to base of posterior margin of ante¬

rior adductor scar. Posterior adductor muscle scar ovate

and indistinct except for its anterior margin, with a blunt

inner ridge running from postero-dorsal shell margin to

antero-ventral corner of posterior adductor scar. Pallial

line indistinct in ventral part, starting at postero-ventral

corner of anterior adductor scar and connecting with

antero-ventral corner of posterior adductor scar without

pallial sinus.

Measurements: See Table 2.

Type Material: The holotype was originally desig¬

nated and illustrated by Tanaka (1959, pi. II, figs. 5 and

6, a specimen “No. 510”). Specimens SFMKT-00389 in

the Kunio Tanakas collection at the Shinshushinmachi

Fossil Museum are with an original label “No. 510”, but

all of the specimens are clearly different from the illus¬

trated holotype. Moreover, we could not find any speci¬

mens corresponding to the holotype illustration in the

collection. We therefore judge that the holotype is lost

and designate a neotype as a conjoined valve preserving

the left hinge dentition (Figures 25-28), SFMKT-00404

(No. 527 in Tanaka, 1959, one of his paratypes); six para-

types excluding SFMKT-00404 designated in Tanaka

(19591 he., SFMKT-00144 (No. 255 in Tanaka, 1959,

pi. II, figs. 1^4), SFMKT-00401 (No. 524, pi. II, fig. 8),

SF MKT-00402 (No. 525, pi. II, fig. 9), SFMKT-00403

(No. 526, pi. II, fig. 7), SFMKT-00405 (No. 528),

SFMKT-00406 (No. 529), and SFMKT-00407 (No. 530).

Tanaka (1959) also designated No. 531 (SFMKT-00408)

as a paratype, but it was identified as another species,

Adulom i/a uch im u raensis .

Type Locality: Akanuda, Matsumoto City, Nagano

Prefecture, central Japan (Loe. 1 in Figure 1).

Table 2. Measurements of Adulomya akanudaensis (Tanaka) from Loc. 1 and 3.

Page 60

THE NAUTILUS, Vol. 131, No. 1

Other Examined Material: In addition to type mate¬

rials from Loc. 1 (SFMKT-00401 to 00407), more than

fifty specimens were collected from Loc. 3 and twenty-

nine well-preserved specimens of them were measured

and examined, SFMCM-0185 to 0191, SFMKT-07227 to

07230, SFMCM-0156 to 0158, 0162, and 0164 to 0171.

Remarks: This species was originally described by Tanaka

(1959) as Calyptogena akanudaensis, which is distinct

from the sympatrie vesicomyid Adulomija uchimuraensis

by its less elongated shell outline. The generic assign¬

ment of this species has been pointed out to be problem¬

atic because its internal shell characters were unknown

(Amano and Kiel, 2011). We reexamined the paratypes

and succeeded in exposing the left valve hinge consisting

of tl iree cardinals, 2a, 2b, and 4b (Figure 28). Moreover,

we obtained many additional specimens from Loc. 3 and

revealed that the right valve hinge is composed of two

cardinals, 1 and 3b (Figure 38). These hinge dentitions

agree well with those o i Adulomya, and are inconsistent

with an assignment to Calyptogena Dali, 1891, which has

three cardinal teeth and a posterior nvmphal ridge on the

right valve.

The reassignment of this species from Calyptogena to

Adulomija is consistent with the temporal distribution of

other vesicomyid species around the Japanese islands,

which was reviewed by Amano and Kiel (2007, 2011),

Amano and Jenkins (201 1), and Amano (2014). Accord¬

ing to them, Adulomija diversified in the middle Miocene

in both the Pacific and the Japan Sea sides, whereas

Calyptogena first appeared in the late Miocene in the

Japan Sea borderland.

Comparisons: It can clearly be ruled out that

Adulomija akanudaensis represents juvenile shells of

A. uchimuraensis, because the former has a much higher

shell than the latter (Figure 45). Moreover, juveniles of

A. akanudaensis have ovate and more inflated shells

with a less protruded anterior margin than the juveniles

of A. uchimuraensis.

Smaller specimens of Adulomya hamuroi Amano and

Kiel, 2011 from the uppermost lower or lowest middle

Miocene in Toyama Prefecture, Japan are similar to

A. akanudaensis in their elongated elliptical shells, but

are different from A. akanudaensis by having a slightly

higher shell with a concave ventral margin. Moreover,

A. akanudaensis has a less stout central cardinal tooth

(1) in the right valve than A. hamuroi and the central

cardinal tooth (2b) in the left valve is not bifid as

A. hamuroi.

Amano and Kiel (2011) pointed out that some speci¬

mens of Adulomija akanudaensis have similar propor¬

tions as A. kuroiwaensis Amano and Kiel, 201 1 from the

uppermost middle or lowest upper Miocene in Niigata

Prefecture, Japan, but A. kuroiwaensis has a more ante¬

riorly situated beak and an expanded posterior part.

Based on the examined specimens of A. akanudaensis

herein, this species has a higher shell than A. kuroiwaensis

(Figure 45), and has a hollow space between the umbo

Figure 45. Relationships between shell length and height

with growth of Adulomija akanudaensis (Tanaka) from Locs. 1

and 3, A. uchimuraensis Kuroda, A. kuroiwaensis Amano and

Kiel, A. hamuroi Amano and Kiel, and Abijssogena kaikoi

(Okutani and Metivier). Measurements of A. uchimuraensis

are from Kanno et al. (1998), those of A. kuroiwaensis and

A. hamuroi are from Amano and Kiel (2011), and those of

Ah. kaikoi are from Krylova et al. (2010).

and the central cardinal tooth (1) of the right valve that is

absent in A. kuroiwaensis .

Adulomija akanudaensis resembles A. chinookensis

(Squires and Goedert, 1991) from the upper Eocene to

lower Oligocene in western Washigton, USA in general

shell outline and having a blunt ridge extending postero-

vent rally from the umbo. A. chinookensis was originally

described as Calyptogena chinookensis , but Amano and

Kiel (2007) revealed its dentition and reassigned it into

the genus Adulomija. Adulomija akanudaensis is different

from A. chinookensis by having a less elongate shell and a

hollow space between the central cardinal tooth (1) and

the nmbo in the right valve.

Adulomya akanudaensis is also similar to Abijssogena

kaikoi (Okutani and Metivier, 1986) living in the Pacific-

side of Japan, in shell proportion (Figure 45) and non-

fusing cardinals (1 and 3b) in the right valve. Abijssogena

kaikoi was originally assigned to the subgenus Ectenagena

Woodring (1938), which was later synonymized to the

genus Adulomija by Amano and Kiel (2007). Krylova

et al. (2010) established the new' genus Abijssogena

including Abijssogena kaikoi and stated that Abijssogena

Y. Miyajima et al., 2017

Page 61

differs from Adulomya by the absence of subumbonal pits

and a pallia] line originating from the ventral margin of

the anterior adductor scar. Adulomya akanudaensis differs

from Abyssogena kaikoi by lacking a pallial sinus and a

bifid posterior cardinal tooth (3b) in the right valve.

Distribution: Middle Miocene Bessho Formation in

Nagano Prefecture, Japan.

Adulomya sp. 1

(Figures 46-53)

Figures 46-53. Adulomya species. 46-53. Adulomya sp. 1 . All specimens are from Loc. 2. 46. Left lateral \iew of inner mold; aas,

anterior adductor muscle scar; KUGSMM01. 47. Bight valve hinge; KUGSMM78. 48. Left valve hinge; KUGSMM66. 49. Left

lateral view ol inner mold; aas, anterior adductor muscle scar; KUGSMM100-6. White arrow shows lack of pallial sinus. 50. Left

lateral view; KUGSMM61. 51. Left lateral view of inner mold; KUGSMM103. 52. Left lateral view of inner mold; KUGSMM41.

53. Right lateral view of inner mold; KUGSMM84. 54. Adulomya uchimuraensis Kuroda from Loc. 1. Left lateral view with inner

mold in part. Scale bars = 10 mm (for all figures).

Page 62

THE NAUTILUS, Vol. 131, No. 1

Description: Shell small for genus (up to S9.9 mm long),

elongate throughout ontogeny (height/length = 0.27-0.44),

posteriorly expanded, equivalve and inequilateral, weakly

inflated (width/length = 0.15-0.30), sculptured by fine

growth lines widening in posterior part. Antero-dorsal

margin nearly straight to broadly concave, gradually

changing to narrowly rounded and slightly protruded ante¬

rior margin; postero-dorsal margin long and straight to

broadly convex, continuing to rounded posterior margin

gradually or a little abruptly at obtuse angle; ventral mar¬

gin broadly arcuate or broadly concave in some specimens.

Beal| low, prosogyrate, situated at 7-21% of shell length

from anterior margin. Lunule and escutcheon absent;

ligament exterior, strong and long, occupying more than

half of postero-dorsal margin. Right valve hinge: anterior

cardinal tooth (3a) reduced; central cardinal tooth (1) thin,

slightly oblique anteriorly from umbo; posterior cardinal

tooth (3b) thick, oblique posteriorly. Left valve hinge: ante¬

rior tooth (2a) thick, subparallel to antero-dorsal shell

margin, connected to central tooth (2b); central tooth (2b)

as thick as anterior tooth (2a), vertical to hinge base; pos¬

terior tooth (4b) as thick as anterior (2a) and central (2b)

teeth, connected to central tooth (2b), oblique posteriorly,

but its distal end unknown. Anterior adductor muscle scar

small and pear-shaped, with a distinct inner rib running

from umbo to just below anterior adductor scar. Posterior

adductor muscle scar indistinct. Pallial line only visible

in posterior part, lacking pallial sinus. Indistinct radial

interior striations visible in anterior part, running from

umbo in slightly posterior direction.

Measurements: See Table 3.

Material Examined: Among one hundred and thirty

collections from Loc. 2, sixteen entirely-preserved spec¬

imens were measured and examined, KUGSMM01, OS,

18, 41, 60, 61, 84, 92, 96, 99, 100, 101, and 103.

Distribution: Only from Sorimachi (Loc. 2), middle

Miocene Bessho Formation in Nagano Prefecture, Japan.

Figures 55. Relationships between shell length and height with

growth of Adulomya sp. 1 from Loc. 2, A. uchimuraensis Kuroda,

and A. chitanii Kanehara. Measurements of A. uchimuraensis and

A. chitanii are from Kanno et al. (1998) and Amano and Kiel

(2011), respectively.

Remarks: The elongate shell and the hinge structures

composed of two cardinals on the right and three cardi¬

nals on the left valve show that the vesicomyid fossils

from Loc. 2 belong to the genus Adulomya. We tenta¬

tively describe them as Adulormja sp. 1 because of the

poor preservation; most specimens are deformed and

compressed inner molds or shells almost dissolved

or replaced by sparry calcite, with the cardinal teeth

unclear. Adulomya sp. 1 was previously reported as

Y. Miyajima et al., 2017

Page 63

Adulomya uchimuraensis (Tanaka, I960; Seki, 1983;

Miyajima et al., 2014), hut is clearly distinguishable

from A. uchimuraensis in having smaller and higher

shells (Figures 54 and 55). Adulomya sp. 1 resembles

A. chitanii Kanehara, 1937 in shell size and outline

(Figure 55), but can be distinguished from A. chitanii

by the lacking of a pallial sinus.

DISCUSSION

Modern vesicomyid species diversity has been explained

from the viewpoints of their bathymetric distribution

(Fujikura et al., 2000), salinity or water temperature

(Watanabe et al., 2013), and different preferences in

hydrogen sulfide concentration at methane seeps (Barry

et al., 1997; Sahling et al., 2002). On the other hand,

little is known about the drivers of fossil vesicomyid

species diversity. It is noteworthy that a total of four

species, Pliocardia? tanakai new species, Adulomya

uchimuraensis, A. akanudaensis , and Adulomya sp. 1,

occur in a single formation. In particular, the former

three species co-occur at the same seep carbonates,

Akanuda and Anazawa limestones (Loe. 1). Such

co-occurrence of more than two vesicomyid species

seems to be rare in ancient seep environments. Although

Kiel and Amano (2010) described three vesicomyid

species, i.e., Adulomya sp. A, Adulomya? sp. B, and

Archivesica redwoodia from a single site (USGS loc.

15399) in the lower Miocene Redwood Formation,

Katalla District, southern Alaska, they are from a silici-

clastic sedimentary rock without seep carbonates.

Modern analogues of such co-occurrence of two or

more species at a single seep site have been recognized

in Saganri Bay (Kojima and Ohta, 1997) and Monterey

Bay (Barry et al., 1997). In Saganri Bay, two sibling spe¬

cies, Archivesica soyoae and A. okutanii (reassigned to

the genus Phreagena by Krylova and Sahling, 2010)

have different preferences in salinity arid temperature

(Watanabe et al., 2013). In Monterey Bay, Archivesica

kilmeri (synonym of soyoae-, Kojima et al., 2004; Okutani

et al., 2009) and Calyptogena pacifica have different

physiological tolerances to hydrogen sulfide concentra¬

tions (Barry and Kochevar, 1998), and these two species

are segregated along sulfide gradients from the center to

the margin of the seeps (Barry et al., 1997).

In the Bessho Formation, such segregation of the

vesicomyid species at seeps could not be recognized

unequivocal lv. In the large-sized seep limestones

(Loc. 1 ), Adulomya uchimuraensis is dominant and ubiq¬

uitous throughout the carbonate bodies and even in the

neighboring siltstone. Autochthonous specimens of

Pliocardia ? tanakai were found by one of the authors

(TN) in die peripheral part of the Anazawa limestone

(Loc. 1), which also contains scattered shells of A.

uchimuraensis. Although the mode of fossil occurrence of

A. akanudaensis at Loc. 1 is unknown, A. akanudaensis

may be mixed with A. uchimuraensis in local shell con-

centrabons as in die small-sized carbonate body at Die. 3.

It is noted that the relative abundances of the three

vesicomyid species are different between Logs. 1 and 3.

In the large-sized seep carbonate bodies at Loc. 1,

Adulomya uchimuraensis dominates throughout the car¬

bonates (more than 200 specimens have been collected),

whereas Pliocardia? tanakai (only total 10 specimens

were obtained by K. Tanaka and the authors) and

A. akanudaensis (only 9 specimens were collected by

K. Tanaka) are rare. In the small-sized carbonate body

at Loc. 3, A. akanudaensis (more than 30 specimens

were collected by the authors) is as abundant as

A. uchimuraensis, but P.? tanakai could not be found.

The sizes of seep deposits are often related to longevity

of fluid-flow history or fluid flux (Luff and Wallmann,

2003; Luff et al., 2004; Nesbitt et al., 2013), and the

larger carbonate size at Loc. 1 suggests a longer fluid-

flow history or a higher fluid flux than Loc. 3. This is also

supported by the difference in the associated other mol-

luscan fossils between these localities. While the seep

carbonates at Loc. 1 contain diverse molluscan fossils

including bathymodioline mussels, which are known

from high-flux seeps (e.g., MacDonald et al., 1989; Olu

et al., 1996), the carbonate at Loc. 3 contains less diverse

mollusks. Moreover, the lithology and carbon isotopic

compositions of the carbonates are also different

between Locs. 1 and 3. The large seep carbonates at

Loc. 1 consist of muddy micrite and caleite veins, show¬

ing low §13C values (—40 to — 36%o; Sato et al., 1993),

whereas the smaller carbonate body at Loc. 3 consists

monotonously of micrite wi th 51 5C values ranging from

—29.8 to +10.5%o. These suggest that the fluid intensity

and composition, as well as longevity or flux, were differ¬

ent between the two seep sites (Peckmann et al., 2009;

Kiel et al., 2014). Namely, an abundance of 1 !C-depleted

void-filling cements, such as sparitic veins in the carbon¬

ates at Loc. 1 , is often attributed to a vigorous, advective

flow, whereas the absence of such early-diagenetic

cements suggests diffusive seepage (Peckmann et al.,

2009; Kiel et al., 2014). The carbon isotopic composi¬

tions of seep carbonates are thought to vary depending

on fluid composition such as thermogenic or biogenic

methane (Whiticar, 1999) or crude oil (Roberts and

Aharon, 1994), or on fluid flux. Therefore, different

preferences in these factors relating to the seep activity

may have been related to the relative abundance of the

three vesicomyid species in the Bessho Formation.

Fluid flux probably also played a role in controlling the

distribution of Adulomya sp. 1. This species is restricted

to Loc. 2, where several cm-sized small carbonate

concretions, having 5UC values as low as — 35%o, are

scattered throughout the siltstone. Although the detailed

study of this locality including carbon isotopic compo¬

sitions of carbonates will be reported elsewhere, the

scattered occurrence of small carbonate bodies suggests

that the seepage was diffusive, with ephemeral and weak

fluid flow (Nesbitt et al., 2013). In contrast, the larger

seep carbonate bodies at Loc. 1 suggest longer fluid-flow

history and a higher flow rate. The size difference

between the seep deposits of Locs. 2 and 3 also suggests

Page 64

THE NAUTILUS, Vol. 131, No. 1

some variation of seep activity, but it cannot be

confirmed because most parts of the carbonate body

at Loc. 3 originated from methanogenesis as well as

methane oxidation.

In summary, the four fossil vesicomyid bivalves in

the middle Miocene Bessho Formation may have had

different preferences for fluid flux rates, fluid composi¬

tion, and longevities among seep sites. The vesicomyid

species diversity in this formation suggests that the diver¬

sification of vesicomyids through the Cenozoic could

have been sustained not only by geographic and bathy¬

metrical separation but also by adaptation to various

seepage conditions.

ACKNOWLEDGMENTS

We are grateful to Yumiko Watanabe (Kyoto University,

Japan) for help in analyzing carbon and oxygen isotopic-

compositions of carbonate samples. We sincerely

appreciate valuable comments and critical reviews by

Steffen Kiel (Swedish Museum of Natural History,

Stockholm), Elena M. Krylova (Russian Academy of

Sciences, Russia), and the editor Jose II . Leal (Bailey-

Matthews National Shell Museum, USA), which help

improve our manuscript. Financial support was provided

by JSPS KAKENH1 (18340165 and 23540548 to TN:

Grant-in-Aid for Scientific Research by Japan Society

for Promotion of Science).

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THE NAUTILUS 131(l):67-75, 2017

Page 67

A new species of South Texas scrubsnail, Praticolella

(von Martens, 1892) (Gastropoda: Polygyridae)

Kathryn E. Perez1

Eli Ruiz

Marco Martinez Cruz

Department of Biology

University of Texas Rio Grande Valley

1201 West University Drive

Edinburg, TX 78539 USA

Russell L. Minton

School of Science and Computer Engineering

University of Houston Clear Lake

2700 Bay Area Boulevard MC 39

Houston, TX 77058 USA

ABSTRACT

The Praticolella of South Texas are highly visible and abundant

snails with a confusing taxonomic history. In this paper, we

provide 16S mitochondrial rDNA and morphological evidence

to distinguish a new species of Praticolella , Praticolella salina,

from southernmost coastal Texas. This native species previously

was considered a distinct race of P griseola, which we demon¬

strate does not occur natively in Texas.

Additional Keywords: mtDNA, Praticolella griseola, Praticolella

mexicana, Cameron County, Texas

INTRODUCTION

Praticolella (von Martens, 1892) are small (7-15 mm

wide), globose, helicoid land snails found in open, grassy

habitats. Two species in this genus, P. griseola (Pfeifler,

1841) and P. mexicana Perez, 2011, have established

populations worldwide via human-mediated transport

(Robinson 1999, Perez 2011). Praticolella sensu stricto

contains ten currently recognized species that occur in

Texas. Six species are found in the Rio Grande Valley of

South Texas, including four native and two non-native

species of Praticolella. The South Texas Praticolella have

a great deal of overlap in habitat, shell shape, color,

aperture shape, and shell banding patterns; indeed, this

region has been called a “great melting pot” for these

snails (Cheatum and Fullington, 1971).

Over the last 150+ years, previous workers have rec¬

ognized a unique population of Praticolella located in

coastal South Texas, referring to it as a unique “race” of

P. griseola (e.g. Orcutt, 1915; Rehder, 1966). In 2011,

Perez described Praticolella mexicana and distinguished

this species occurring in Texas from P. griseola and

P. berlandieriana (Moricand, 1833). Phylogenetic work

1 Author for correspondence: [email protected].

by Perez (2011) based on mtDNA sequences established

that a few individuals identified as P. griseola from

Cameron County Texas formed a distinct clade; with

only a single population represented in that study, that

author declined to establish a formal distinctive taxo¬

nomic status for that population. This population was

also found to be distinct using geometric morphometries

(Perez, 201 1). In the present study, we sampled addi¬

tional populations of Praticolella from coastal Cameron

County, Texas, and used anatomical and genetic data to

determine that these populations represented a previ¬

ously unrecognized, distinct species.

MATERIALS AND METHODS

Collections and Molecular Methods: Representatives

of the populations in Cameron County were collected by

hand and individuals were frozen at — 20°C prior to DNA

extraction. We amplified the mitochondrial 16S rDNA

gene of twenty individuals from four of these populations

(Figure 1, Table 1) using the degenerate 16sar-deg and

16sbr-deg primers described in Perez (2011). Methods for

DNA extraction and PCR also follow Perez (2011), and

Sanger sequencing was carried out by Beckman Coulter

Genomics. Contigs were assembled in SeqMan Pro

(DNASTAR 2014. SeqMan Pro®. Madison, WI) and

added to the sequences used in Perez (201 1). The dataset

was aligned using MUSCLE 3.7 (Edgar, 2004) followed

by elimination of poorly aligned positions in Gblocks

0.91b (Castresana 2000) implemented at Phylogeny.fr

(Dereeper et al. 2008) (http://phylogeny.lirmm.fr/phylo_

cgi/index.cgi). We used jModeltest (2.1.7) (Guindon and

Gascuel, 2003; Darriba, et al. 2012) to select TIM1 + I+G

(Posada 2003) as the best model for our data. Maximum

likelihood analysis and 1000 bootstrap replicates were car¬

ried out in Garli 2.01 (Zwickl, 2006). Base frequencies and

substitution rate categories were estimated from the data.

Species Delimitation Analyses: We used three

methods to assess whether our labeled clades represented

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THE NAUTILUS, Vol. 131, No. 1

Figure 1. Map with sampling sites lor Cameron County populations included in the molecular and soil analyses (Table 1 and

Figure 2). The location of Cameron County Texas is depicted in gray in the inset map. State highways are shown as gray lines in

the Cameron County map.

species under the phylogenetic species concept (PSC).

Under the PSC, species are both the smallest units for

which phylogenetic relationships can he reliably inferred

(Baum and Shaw, 1995) and entities residing at the tran¬

sition between evolutionary relationships that are best

reflected as reticulate genealogical connections (Goldstein

et al., 2000). With the Species Delimitation Plugin (SDP)

(Masters et al., 2011) in Geneious 8 (Biomatters Ltd.,

Kearse et al., 2012), we calculated Rosenberg s P(ab) to

test the reciprocal] monophvly of each labeled clade and

its closest clade (Rosenberg, 2007). Rejection of the null

hypothesis suggests genealogical separation of distinct

taxa versus monophyly arising randomly according to

a Yule model. Significance was determined following

Rosenberg (2007). The SDP also assessed the probability

of assigning a given individual to its member clade in two

ways (Ross et al., 2008). A strict probability was deter¬

mined for placing an individual into the correct clade

while not placing it into the sister clade, and a liberal

probability was calculated for placing an individual into

either the correct clade or sister clade (Masters et al.,

201 1). We also calculated the genealogical sorting index

(GSI) for each labeled clade in our phylogeny. The GS1

statistic quantifies the degree of exclusive ancestry for

identified groups in a rooted tree and tests whether it is

greater or less than that expected by chance. Significant

results suggest that a priori groups do not represent

a single mixed genealogical ancestry. We employed a

GSI web service (http://moleeularevoIution.org/software/

phylogenetics/gsi/) and assessed significance at a— 0.05

using 10,000 tip label permutations on our fixed topology.

Finally, we used the Poisson tree processes (PTP) model

(Zhang et al., 2013) to assess whether the number of

substitutions between our labeled clades was significantly

higher than that within those same clades; significantly

more substitutions between clades implies that they repre¬

sent separate phylogenetic species. This method does not

require an ultrametric phylogeny nor an evolutionary time

context. We used an online likelihood implementation of

PTP (http://species.h-its.org/pqV) with default settings.

Morphological Examination: We collected five mea¬

surements from each of 42 individuals, measured to the

nearest 0.1 mm with digital calipers: maximum shell

height parallel to the axis of coiling, maximum shell width

peipendicular to the axis of coiling, maximum aperture

width, aperture height perpendicular to aperture width

measurement, and maximum umbilicus diameter. Only

adult specimens with complete reflected lips were mea¬

sured. The number of whorls was estimated using the

method described by Cheatum and Fullington (1971: 15,

fig. le) to the nearest 0.25 of a whorl at 20x magnifica¬

tion. This method counts each whorl as a complete spiral

turn of the shell. A stacked composite image of the

holotype shell was assembled using Helicon Focus 6.7.1

(Helicon Soft Limited). To relax snails for dissection, snails

were drowned in room temperature water for 30 minutes,

followed by incubation for 90 minutes at 37°C

(Kruckenhauser et al., 201 1). Following relaxation snails

were preserved in 70% ethanol until dissection. Soft tissues

K.E. Perez et al., 2017

Page 69

Table 1. Locality and collection information for populations examined in this study for molecular analysis, soil analysis, and

additional material examined, included from Perez 2011. *At this site only diy shells of P. salina were present. Specimens are

deposited at the Academy of Natural Sciences of Philadelphia Drexler University (ANSP). ANSP numbers beginning with “A" are

lots preserved in alcohol. Field Museum of Natural History accession is coded FMNH. Latitude and longitude presented in decimal

degrees. Cameron County Population Numbers are those labeled on Figure 1.

Page 70

THE NAUTILUS, Vol. 131, No. 1

were removed from the shell and a mid-sagittal incision

was used to expose the internal anatomy. Connective

tissue was removed followed by separation of the genitalia.

All structures were photographed in water.

Soil Sampling: To determine the soil salinity in the

habitat of this species, soil samples were collected at four

of the collection localities for live snails from Cameron

County (Sites 1, 2, 3, and 5 from Table 1). Small samples

of soil were collected by a gloved hand covering the

entire local extent of the population into a single, 5 L

collection. These samples were mixed in a plastic bucket

and a subsample was sent to the University of Louisiana

at Monroe Environmental Analysis Laboratory for quan¬

tification of all extractable elements. Soil descriptors

followed Soil Survey Division Staff (1993).

RESULTS

Twenty new 16S sequences (GenBank KX431997-

KX432016) from four populations of the new species

P. salina were generated. Maximum likelihood analysis

of 436 bp of IBS mt sequences of 1 10 individuals of nine

putative species of Praticolella yielded a single tree

(log likelihood = —4465.5927; Figure 2) with an overall

tree topology similar to that found by Perez (2011).

Outgroups included in the analysis were representatives

of the other genera of Polygyrini included in Perez

(2011): Lobosculum pustuloides (Bland, 1858); Polygyra

septenwolva Say, 1818; Polygyra cereolus (Miihlfeld,

1816); Daedalochila hippocrepis (Pfeiffer, 1848); Linisa

| exasiana (Moricand, 1833); and Millerelix mooreana

(Wi.G. Binney, 1858). Species-level clades were well

supported but relationships among these taxa had little

bootstrap support. Two putative species-level clades

(monophvletic groups identified by the species delimitation

analyses conducted) we recognized currently lack names:

an unnamed species from Soto de la Marina, Tamaulipas,

Mexico, herein referred to as “Soto”; and an unnamed

species from an introduced (greenhouse) population in

Florida, USA, herein referred to as “Florida”. Three other

nominal species (P. taeniata Pilsbry, 1940; P. pachylonm

(Menke in Pfeiffer, 1847); and P. Candida Hubrieht, 1983)

appeared to form a single species-level clade from South

Texas, referred to herein as the “South Texas Clade”. A

weakly supported clade (54%) suggested a close relation¬

ship between P. salina and the Florida population. The

P. salina clade had some internal population-level molec¬

ular structuring with individuals from each population

appearing in the various shallow clades with the

exception of the South Padre Island individuals which

are separate.

We tested our nine labeled species-level clades

(Figure 2) using three species delineation methods.

Based on Rosenberg’s P(Ab)> the SDP supported recog¬

nition of seven of our nine labeled clades as reciprocally

monophvletic taxonomic entities (Table 2 and Figure 2).

The Praticolella berlanderiana clade and South Texas

Clade had non-significant P(abi values. Probabilities of

assigning individuals to their correct clades varied from

59-95% under the “strict” method and 87-99% under

the “liberal” method. The clade representing the new

species had probabilities of 92% and 99% under the

“strict” and “liberal” criteria respectively. All nine labeled

clades possessed significant GSI values (p<0.05),

suggesting no evidence of mixed ancestry in any group.

The maximum likelihood PTP solution identified six of

our labeled clades as possible phylogenetic species:

P. berlandieriana; P. trimatris; South Texas Clade; Soto;

Florida; and P. salina. These species were supported

by all three species delineation methods, however,

P. mexicana , P. griseola , and P. flavescens were not sup¬

ported by PTP, perhaps because of unequal sampling

or unrecognized diversity in these clades.

Soils at Site 1 (tvpe locality) had a pH of 7.67, a salinity

of 1 1 .6 parts per thousand (ppt), and contained 0.89%

organic matter. Across all sites, pH ranged from 7.13 to

8.33, salinity from 0.42 to 22.9 ppt, and organic matter

from 0.13% to 1.59%. This indicated that P. salina was

collected in areas with neutral to moderately alkaline

mineral soils. The salt marsh sites (sites 1 and 3) were

considered highly saline, while the dune (site 2) and

agricultural (site 6) sites were considered non-saline.

SYSTEMATICS

Class Gastropoda Cuvier, 1791

Family Polygyridae Pilsbry, 1930

Genus Praticolella von Martens, 1892

Dorcasia Binney, 1878: 356.

Praticola Strebel and Pfeiffer, 1880: 38 [non Swainson, 1837]

Praticolella von Martens, 1892: 138.

Type Species: Praticola ocampi Strebel and Pfeiffer,

1880 (= Helix ampla Pfeiffer, 1866)

Praticolella salina new species Perez and Ruiz, 2017

(Figures 4-1 1)

Helix griseola Pfeiffer, 1841. — Binney, 1857: pi. 49 fig. 2,

pi. 72 fig. 20.

Praticolella griseola (Pfeiffer, 1841). — Pilsbry, 1940: 690

(misidentification in part), fig. 425; Webb, 1951:

140, pi. 48 fig. 30; Rehder, 1966: 290-291 (misiden¬

tification in part), fig. 20; Cheatum and Fullington,

1971: 38-39 (misidentification in part), figs. 2, 12.

Neck, 1977: (misidentification in part).

Diagnosis: Peristome reflected without inner thickening

and narrow throughout, unique among Texas Praticolella ;

lower surface of body whorl brown with a single to several

white bands; shell wider than high.

Description: Shell large for Praticolella, narrowly umbil-

icate, depressed, brown with white pigmented stripes.

Peristome mostly white, barely reflected at parietal wall

but heavily reflected at umbilicus, partially obstructing

K.E. Perez et al., 2017

Page 71

P. mexicana

P mexicana Andros Island. Bahamas

P. mexicana Andros Island, Bahamas

P mexicana Andros Island. Bahamas

P mexicana Puente San Rodrigo COAH

P. mexicana Diente, NL

P mexicana Diente, NL

P. mexicana from USDA

P. mexicana from USDA

P. mexicana Andros Island. Bahamas

P mexicana from USDA

P mexicana from USDA

P mexicana from USDA

P. mexicana from USDA

r P mexicana Tamasopo, SIP

* P. mexicana Diente. NL

P. mexicana Anahuac. NL

P. mexicana Tamasopo, SLP

P mexicana Key Largo. FL

P mexicana 2 km N Agua Buena, SLP

P mexicana Dominican Republic

P. mexicana Saltillo, NL

P. mexicana San Rafael, VC

P. mexicana Tamasopo, SLP

P mexicana 2 km N Agua Buena. SLP

P mexicana Linares, NL*

P mexicana from USDA

P mexicana S. San Fernando, TMP

P mexicana from USDA

P mexicana from USDA

- P. mexicana Diente. NL

| P mexicana S of Ciudad Victoria, TMP

_ P mexicana S. of Ciudad Victoria, TMP

94 l P mexicana S of Ciudad Victoria, TMP

r P mexicana Rio Frio, TMP

_ r P mexicana Rio Fno, TMP

79 ' P. mexicana Rio Frio, TMP

| P griseola Jimenez, TMP

' P griseola Jimenez. TMP

- P. griseola Vera Cruz, VC*

- P griseola La Mancha, VC

- P. griseola Vera Cruz, VC* p griSPOlO

1 P. griseola N of Vera Cruz, VC

I P griseola San Rafael, VC

ij^P griseola Tula. NL

— - P griseola Lake Co. FL

- P griseola N of Vera Cruz, VC

— P griseola N Papantla, VC

P. sp Soto de la Manna, TMP

sp. Soto de la Marina, TMP SotO

sp Soto de la Marina, TMP

P fla\/escens 9 km N Papantla. VC*

P flavescens 9 km N Papantla, VC*

— P flavescens Tampico. VC

P flavescens 7 km S Tamapache, VC

P flavescens 9 km N Papantla, VC*

h£

&

P. flavescens

r P. trimetris, Roma, TX

P. trimatris

L P trimatris, Roma, TX

I P sp Camp Perry, TX

P P sp Camp Perry. TX

1" P sp Camp Perry, TX

' P. sp S of Weslaco. TX

P sp 5 km NE Three Rivers. TX

• P sp 5 km NE Three Rivers. TX

P sp 2 km S San Fernando. TMP

P. sp Raymondville, TX

P. sp N of Raymondville, TX

P sp N of Raymondville, TX

P sp Raymondville, TX

P sp Raymondville, TX

■ P sp. 2 km S San Fernando. TMP

P sp 2 km S San Fernando, TMP

P. sp. 2 km S San Fernando, TMP

| P berlandienana 9 km N New Braunfels, TX*

P bertandieriana 9 km N New Braunfels, TX*

P bertandienana 12 km E of Blanco. TX

South Texas Clade

99

P. berlandieriana

| P. salina 8 km S Port Isabel, TX*

J P. salina 8 km S Port Isabel, TX*

*- P salina 8 km S Port Isabel, TX*

Y2 P salina 8 km S Port Isabel, TX*

P salina 8 km S Port Isabel, TX*

- P. salina 5 mi S Port Isabel, TX*

■ P salina 2.5 km W Laguna Vista. TX

| P salina 5 km S Port Isabel. TX*

I _ P salina 2.5 km W Laguna Vista, TX

' P sp just W Laguna Vista. TX

P salina 8 km S Port Isabel, TX*

P salina South Padre Island, TX

P. salina South Padre Island. TX

P. salina South Padre Island, TX

P salina South Padre Island, TX

P salina 8 km S Port Isabel. TX*

P. salina 8 km S Port Isabel, TX*

P. salina 8 km S Port Isabel, TX*

P salina 8 km S Port Isabel, TX*

P salina 8 km S Port Isabel, TX*

P. salina Port Isabel High School, TX

P. salina Port Isabel High School, TX

P salina Port Isabel High School, TX

_ j P sp Lake Co FL

* P sp Lake Co. FL

P salina

Florida

Figure 2. Maximum likelihood phylogeny based on 436 bp of 16S mt sequences of 1 10 individuals. Only Praticolella sensu stricto

are shown. Bootstrap values >50% shown below the nodes. Individuals marked with * were collected from type locality. Outgroups

are omitted from the figured tree.

Page 72

THE NAUTILUS, Vol. 131, No. 1

Table 2. Results f roin the Species Delimitation Plugin

analysis. Clades correspond to those in Figure 2. Ps and Pi

are probabilities of correct identification under strict and liberal

criteria respectively. Asterisks (*) signify significant values of

Rosenberg’s P(AB) and thus separate taxonomic entities by that

measure. Clades with significant GSI values and identified as

possible phylogenetic species by PTP are also indicated.

umbilicus in most individuals. Aperture slightly lunate

with light parietal callus. Suture smooth but uneven

where intersected by growth lines. Protoconch smooth,

with longitudinal growth lines (radial lines) appearing by

the second spire whorl. Spire and body whorls white

above a single translucent, light-brown band around the

periphery; up to six additional white stripes below that

translucent band. Umbilicus outlined by a single translu¬

cent, light-brown band often followed by a white pigmented

band. Mean shell height 9.10 ± 0.48 mm, width 12.21 ±

0.68 mm, height/width ratio 0.75; mean aperture height

6.4 2± 0.66 mm, width 6.42 ± 0.14 and height/width

ratio 0.88 (Table 3).

Body color brown in life. Largest branch of divided

penial retractor muscle inserted on apex of penis. Two

smaller branches attached to penis with vas deferens pass¬

ing between them (Figure 3). Vas deferens of consistent

diameter across its length. Penis bipartite with one

smooth bulb and distinct appendix. Penial appendix, in

the unextended state, slightly narrower at penial attach¬

ment, widening and becoming bulbous, about one-half

total penial width. Distal end of the penial appendix

slightly hooked. Epiphallus noticeably smaller in diameter

than the penis, with the vas deferens at the terminal end;

flagellum absent. Bursa copulatrix thin, clavate, widening

slightly at the terminus. Ovotestis appears as a sponge¬

like, irregular mass.

Figure 3. Internal anatomy of specimen from Cameron County,

TX. ANSP A24739. AG, albumen gland; BC, bursa copulatrix;

C, carrefour (spermatheca and fertilization pouch complex);

EP, epiphallus; G, genital pore; HD, hermaphroditic duct;

OT, ovotestis; P, penis; PA, penial appendix; PRM, penial retractor

muscle; SO, spermoviduet; \( vagina; VD, vas deferens.

Type Material: Holotype, ANSP A24736; Paratypes,

ANSP 467509 (35 individuals), all from type locality.

Type Locality: 8 km south of Port Isabel on HWY 48,

Laguna Atascosa National Wildlife Refuge, Cameron

County, TX. 25.9957 N, -97.311 W, (8 November 2014,

coll. K. E. Perez and E. Rniz).

Distribution and Habitat: Vegetated dunes and sands

and clay soils on South Padre Island and coastal Cameron

County, Texas. These locales are associated with Gulf

Coast saline prairie habitats in the South Texas Lomas

Table 3. Shell measurements for the Praticolella species under consideration. Only adult shells with a full lip were measured.

Measurements for P. griseola (n=36) are from (Perez 2011) and P. salina (n=42) from the present study. Values present are the range

of values, mean, and standard deviation. Measurements taken: shell height (h), width (w), aperture height (aph), aperture width (apw),

umbilicus width (umb), and number of whorls (# of whorls).

K.E. Perez et a]., 2017

Page 73

Figures 4—11. Shells of Praticolella salina new species. 4-8. Holotype, ANSP A24736, f rom tvpe locality: 8 km S of Port Isabel on

HW 48, Laguna Atascosa National Wildlife Refuge, Cameron County, Texas, 8 Nov 2014, K.E. Perez, E. Ruiz, lateral, basal, and

apical views of the shell, close up of suture and embryonic whorls, w=13.60 mm, h=10.03 mm, 5.5 whorls. 9. ANSP 467487; UTRGV

Coastal Studies Lab, Isla Blanca Park, south end of South Padre Island, Cameron County, Texas, 19 Oct 2014. K.E. Perez,

D. Deshommes, w=10.06 mm, h=7.64 mm, 5.0 whorls. 10. ANSP 467487; UTRGV Coastal Studies Lab Isla Blanca Park, south

end of South Padre Island, Cameron County, Texas, 19 Oct 2014. K.E. Perez, D. Deshommes, w=10.88 mm, h=8.59 mm, 5.5 whorls.

11. ANSP A24739, 2.5 km W of the water treatment f acility at Laguna Vista, S side of HWY 100, Cameron County, Texas, 29 March

2016, E. Ruiz, w=11.87 mm, h=9.23 mm, 5.25 whorls.

ecological system (Natureserve, 2016), a rare plant

community recognized by Texas Parks & Wildlife. Indi¬

viduals have been found in Dune sand, Harlingen clay,

Point Isabel clay, Lomalto clay, and Laredo silty clay

loam soil types. Dominant vegetation in the clay soils

includes shoregrass ( Monanthochloe littoralis ), bushy

seaside tansy ( Borrichia frutescens ), and Florida /

gutta-percha Mayten ( Maytenus phyllanthoides); all are

salt tolerant species. Snails were found crawling or esti¬

vating on cactus ( Opuntia sp.) at Sites 1 — 4, Site 5 was

recently modified to citrus orchards and cornfields, with

no cactus present. This species appears to have a very

limited distribution that is likely reduced from its previ¬

ous extent. We find only dry shells of P. salina farther

inland and in close proximity to extant P. mexicana col¬

onies. The species likely extends into coastal, northern

Tamaulipas, Mexico as well, but that area has not been

sampled by the authors.

Etymology: From Latin, salinus, salty (derivative of sal),

in reference to the species’ unusual occurrence in highly

saline terrestrial habitats.

Comparisons with Other Praticolella: The shell of

P. salina is distinct from that of P. griseola in being larger,

wider and less globose, and lacking a diagnostic cinnamon-

brown pigmented band. The aperture of P. salina is also

wider than high compared to the nearly round aperture

of P. griseola. Praticolella salina can be distinguished

from shells of the South Texas Praticolella elade members

by its thin versus thickened and deeply reflected peri¬

stome. It can be distinguished from P. mexicana in always

Page 74

THE NAUTILUS, Vol. 131, No. 1

possessing some white pigmented bands that follow the

axis of coiling; none of them, however, run against the

axis of coiling or have a pattern of alternating white,

pigmented and brown, unpigmented, broken “rays” running

perpendicular to the axis of coiling as is often the case in

P. mexicana.

The penial appendix of P. salina is distinctive as it is

distally clavate, hooked, and about half the width of the

penis. In P. mexicana, this structure is equally wade along

its length, lacks any hook, and is slightly less than the

penile width. The bursa copulatrix of P. salina is clavate,

only slightly wider at the distal end than at the insertion

into the vagina. This structure is distinguishable from

that of the South Texas clade which is reniform (Vanatta,

1915), and from both P. mexicana and P. berlandieriana

(Webb, 1967), which have expanded spatulate distal ends

that taper to narrow insertion points.

Remarks: Perez (2011) reviewed the turbulent taxo¬

nomic history of Praticolella from southern Texas and

northern Mexico, especially as it relates to nominal

P. griseola from Cameron County, Texas. Praticolella

griseola was originally described from Veracruz, Mexico,

by Pfeiffer (1841). Orcutt (1915) first considered

P. griseola of Texas to be distinct instead of an example

of a polymorphic species. Pilsbry (1940) figured P. salina

from Brownsville, Texas, as P. griseola and noted that

Brownsville specimens were larger and banded differ¬

ently than the type specimen. Rehder (1966) compared

P. griseola from throughout its range and considered the

Brownsville population to be a distinct race, character¬

ized bv large specimens with sharply defined color

bands. In their review of Texas Praticolella , Cheatum

and Fullington (1971) reviewed P. griseola. The descrip¬

tions, distribution, and measurements given by Cheatum

and Fullington for that latter species represent P. salina

as well as other South Texas species. Neck (1977) revised

nomenclatural and distribution records for P. griseola of

previous authors, and restricted P. griseola in Texas to

Cameron County near Brownsville and Laguna Atascosa

National Wildlife Refuge. Herein we consider all of

these treatments of P. griseola in South Texas to be con¬

sistent with and indicative of P. salina.

By restricting its distribution to southern Texas (possibly

south to Tamaulipas), we aim to emphasize the separation

of Praticolella salina and P. griseola evidenced by morpho¬

logical and molecular data. Praticolella griseola sensu

stricto is a species from the Gulf Coastal Plain of south-

central Mexico that has been moved through human

activity with established populations in Alabama, Florida,

and I xmisiana. Any occurrence of time P. griseola in Texas

is therefore considered an introduction, not a native and/

or remnant population. Additional historical records of

P. griseola in Texas have been or should be reassigned to

other species, including P. mexicana. As such, we have

limited our synonymy to those works that clearly illustrated

a shell we consider to be P. salina. Other works listing

P. griseola ambiguously from Texas may represent P. salina ,

but without additional evidence they were excluded.

We often find Praticolella salina occurring with other

Praticolella species. In Brownsville, for example, we

confirmed Pilsbry s (1940) observation that it occurs with

P. taeniata. Similarly, we have also found P. salina within

a few meters of P. mexicana , where the former was in

native habitat and the latter in the grassy verge of a

roadway. This is reminiscent of how other Praticolella

species co-occur, such as P. griseola and P. flavescens

in central Mexico.

The present study with extensive sampling in Cameron

County found only eight populations of Praticolella salina

(seven with living individuals present) in a coastal region

with rapid habitat modification due to housing and

business developments. This finding is typical of land

snails, one of the most diverse, relatively poorly known,

and imperiled groups of animals globally (Lydeard

et ah, 2004).

ACKNOWLEDGMENTS

We thank the University of Texas Rio Grande Valley’s

(UTRGV) Science Education Grant #52007568 funded

by tlie Howard Hughes Medical Institute, ADVANCE

Institutional Transformation Grant (NSF# 1209210),

UTRGV Faculty Research Council, Undergraduate

Research Initiative, and College of Sciences for financial

support. This work was supported in part by the National

Science Foundation (under grant HRD-1463991). Any

opinions, findings, and conclusions or recommendations

are those of the authors and do not necessarily reflect

the views of NSF. We thank Frank Judd for assistance

with plant identification, Zen Faulkes for use of photo¬

graphic equipment, Patrick Marquez for anatomical

photographs, Tim Pearce for a critical review, and Paul

Callomon for specimen deposition. We also thank Ned E.

Strenth, T. Glenn Littleton, Victoria Garcia Gamboa,

Ruth Lopez, Didier Deshommes, and Norma Allie Perez

for assistance with collections.

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Castresana, | 2000. Selection of conserved blocks from multiple

alignments for their use in phylogenetic analysis. Molecular

Biology and Evolution 17: 540-552.

Cheatum, E.P. and R.W. Fullington. 1971. The Aquatic and

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of Natural History 1: 1-74.

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THE NAUTILUS 131(l):76-86, 2017

Page 76

A new genus and species of Neomphalidae from a hydrothermal

vent of the Manus Back- Arc Basin, western Pacific

(Gastropoda: Neomphalina)

Shuqian Zhang

Suping Zhang1

Institute of Oceanology

Chinese Academy of Sciences

Qingdao 266071, CHINA

ABSTRACT

Lamellomphalus manusensis new genus, new species is

described from a hydrothermal vent site of the Manus Back-

Arc Basin. The familial assignment is based on morphologies

of shell and external anatomy. The new taxon is superficially

similar to some members of Peltospiridae McLean, 1989

in general shell shape, but differs from all peltospirids in

having sex dimorphism and presence of a copulatory organ.

Lamellomphalus manusensis is characterized by possessing

haliotiform shell with some degree of coiling, which could

be considered as an intermediate form in the family

Neomphalidae McLean, 1981, between species with regu¬

larly coiled shells ( Cyathermia Waren anil Bouehet. 1989;

Lacunoides Waren and Bouehet, 1989; Planorbidella Waren

and Bouehet, 1993, and Solutigyra Waren and Bouehet,

1989) and limpet-like shells ( Neomphalus McLean, 1981

and Symmetromphalus McLean, 1990). This feature thus

distinguishes the new taxon from other neomphalids. A phy¬

logenetic reconstruction based on cytochrome c oxidase I gene

(COI) also supports its placement within Neomphalidae.

Additional keywords: Gastropoda, Neomphaloidea, chemosyn-

thetic environment, new taxon

INTRODUCTION

The Manus Baek-Are Basin is of particular biological

interest due to its location between the biologically well

studied Mariana Trough and the vent communities of

tin1 North Fiji and Fan Back-Arc Basins. That special

geographical environment yields many interesting and

new gastropods, attracting the interest of many scientists

(e.g. Desbruyeres and Laubier, 1989; Beck, 1991,

1992a, 1992b, 1993; Bouehet and Waren, 1991; Waren

and Bouehet, 1993).

Neomphalina (Waren and Bouehet, 1993) are a group

of gastropods that inhabits ehemosynthetic environ-

1 Author for correspondence: [email protected]

ments (Desbruyeres et ah, 2006; Sasaki et ah, 2010) and

sunken wood (Hess et ah, 2008). Among them,

Neomphalidae is a particular family that by far is con¬

sisting of six genera and eight species, known from East

Pacific Rise (Waren and Bouehet, 1989), Galapagos

Rift (McLean, 1981; Waren and Bouehet, 1989), Lau

Basin (Waren and Bouehet, 1993), Axial Seamount

(Waren and Bouehet, 2001) and Mariana Back-Arc Basin

(McLean, 1990).

In June 2015, during a scientific investigation carried

out by the Institute of Oceanology, Chinese Academy of

Sciences (IOCAS), several limpet-shaped gastropods

were collected in the Manus Back-Arc Basin by a dive

of the ROV Faxian (based on mother ship R/V Kexue).

Observations on their shell, radula features and exter¬

nal anatomy confirmed that they represent a new

genus and a new species belonging to the family

Neomphalidae McLean, 1981. In present study, we

describe and illustrate this new taxon, comparing it to

its closest relatives.

MATERIALS AND METHODS

More than 130 specimens were collected during single

dive of the ROV Faxian (IOCAS) in June, 2015, at a

hydrothermal vent site in the Manus Back-Arc Basin.

This vent field is composed of both fissure areas and

more active zones with small anhydrite and tall sulfide

and silica chimneys ejecting greyish-black fluids (see

Fourre et ah, 2006 for details). The entire area is par¬

tially colonized by vestimentiferan worms (Siboglinidae)

associated with the large gastropods Ifremeria nautilei

Bouehet and Waren, 1991, mussels, shrimps and

galatheid crabs.

The specimens described herein were collected by

the mechanical arm of the ROV Faxian in the course

of sampling the rock where specimens were attached.

The materials were fixed in 99.5% ethanol directly after

collection. Preserved specimens were brought to Marine

S. Zhang and S. Zhang, 2017

Page 77

Table 1. Shell measurements of Larnellomphalus manusensis

new species.

Biological Museum, Chinese Academy of Sciences

(MBMCAS), for further study. Shell measurements

were taken with a caliper with accuracy of 0.1 mm

(see Table 1 ).

Scanning Electron (SEM) and Light Microscopies

(SEM): Shell and soft part morphologies were exam¬

ined via both light microscopy and SEM, and the radula

by SEM alone. Soft parts of two specimens were critical-

point dried for SEM studies. For SEM studies of

radulae, radular sacs were removed and placed in

10% NaOH solution for 7-8 hours. The radulae were

then dehvdrated through an ethanol series and laid on

a cover slip to air-dry. Samples were coated with gold

and examined under a Hitachi S-3400N scanning electron

microscope. Type material was deposited at MBMCAS,

Qingdao, China.

Molecular Analyses: Five specimens were subjected

to molecular analysis. Genomic DNA from each individ¬

ual was extracted with the Column Genomic DNA Isola¬

tion Kit (Beijing TIANGEN, China) according to the

manufacturer’s instructions. DNA was eluted in elution

buffer and stored at — 20°C until use. The COI region

was amplified by polymerase chain reaction (PCB) using

the primers LCO1490 (forward: 5'-GGTCAACAAAT

C ATA A AG ATATTGG-3' ) and HC02198 (reverse: 5'-TTA

ACTTCAGGGTGACCAAAAAATCA-3') (Folmer et ah,

1994). PCB reactions were carried out in a total volume

of 50 pL, including 2 mh DNA template, 1.5 mM

MgCh, 0.2 mM of each dNTPs, 1 pL of both forward

and reverse PCB primers, 10 x buffer and 2.5 U Taq

DNA polymerase. Thermal cycling was performed under

the following conditions: 95°C for 3 min (initial denatur-

ation), followed by 35 cycles of 95°C for 30s (denatur-

ation), 42°C for 30s (annealing), 72°C for 60s (extension)

and a final extension at 72°C for 10 min. PCB products

were verified on a Gel Bed-stained 1.5% agarose gel

and purified with the Column PCB Product Purification

Kit (Shanghai Sangon, China). Purified products were

sequenced in both directions using the BigDye Termina¬

tor Cycle Sequencing Kit (ver. 3.1, Applied Biosystems)

and an AB PBISM 3730 (Applied Biosystems) automatic

sequencer. Sequence alignments were generated using

Clustal X (Larkin et ah, 2007). For phylogenetic analy¬

ses, COI sequence from present study and those from

GenBank were used (see Table 2). Neighbor-joining

(NJ) tree was performed by MEGA 6.06 (Tamura

et ah, 2013), using Kimura 2-parameter (K2P) model

(Kimura, 1980). Bootstrap analyses were performed with

1000 replications.

SYSTEMATICS

Superfamily Neomphaloidea McLean, 1981

Neomphalidae McLean, 1981

Table 2. Works from which the COI sequences derived.

Page 78

THE NAUTILUS, Vol. 131, No. 1

Lamellomphalus new genus

Type Species: Lamellomphalus manusensis new spe¬

cies, by original designation.

Diagnosis: Shell haliotiforin. Coiled earlier whorl off¬

set to posterior right. Protoconch and first teleoconch

whorl with coiling axis parallel to adult aperture.

Protoconch surface sculptured with irregular network

of low ridges. First 1.2 teleoconch whorl rounded, sculp¬

tured with weak axial threads; subsequent teleoconch

whorl rapidly expanding, with developed reticulated

sculpture. Operculum present, mutispiral with wide

free edge. Neck short, dorso-ventrally compressed.

Mouth opening triangular; snout apieally strongly

bilobed and drawn out laterally into points. Cephalic

tentacles short, postero-laterally oriented, left tentacle

of male greatly enlarged, serving as copulatory organ,

deep ventral sperm groove connecting with groove

on left side of neck. Epipodial tentacles present poste¬

riorly and laterally. Ctenidium bipectinate, afferent

membrane absent; efferent axis merged with floor of

mantle cavity by thickened efferent membrane; gill

lamellae elongate. Mantle cavity open anteriorly. Rad-

ula rhipidoglossate, has a formula of (ca. 10)+4+l-|-4-l-

(ca. 10), cusps of inner three lateral teeth similar

to those of rachidian teeth with smooth cutting edges,

fourth lateral teeth strongly serrate on outer edge; marginal

teeth with long, broad shafts, cusp edges deeply divided

into about 20 serrations.

Etymology: The name of new genus refers to the

lamellae-like structures formed on shell periostracum.

Remarks: Lamellomphalus superficially resembles some

members Peltospiridae (e.g. Hirtopelta hirta McLean,

1989; Ctenopelta porifera Waren and Bouchet, 1993,

and Hirtopelta tufari Beck, 2002) in having haliotiforin

shell with coiling axis of earlier whorls parallel to final

aperture, but differs from them by displaying sexual

dimorphism and a copulatory organ, lack of gill affer¬

ent membrane and by the non-serrated cusps of the

rachidian and lateral teeth. Within Neomphalidae,

Cijathermia, Lacunoides, Planorbidella, and Solutigyra

can be clearly separated from Lamellomphalus by

their regularly coiled shells. In addition, Cijathermia

and Lacunoides differs from Lamellomphalus by hav¬

ing a left tentacle with closed sperm groove and

two proximal cirri, and by serration on cusps of

rachidian and lateral teeth; Planorbidella and Solutigyra

mainly differ by having cephalic tentacles of equal

size in both female and male. Neomphalus and

Symmetromphalus somewhat resemble Lamellomphalus

in their limpet-shaped shell. However, Neomphalus

and Symmetromphalus can be differentiated from

Lamellomphalus by having the coiling axis of earlier

whorls perpendicular rather than parallel to the

adult aperture.

Lamellomphalus manusensis new species

(Figures 1-32)

Description: Shell (Figures 1-6) of medium size for

family (maximum length 8.9 mm for female and 6.6 mm

for male), shell color white. Periostracum olive-green,

extending beyond shell margin. Shell haliotiforin, profile

moderately depressed. Spire small, appressed to the pos¬

terior right side of the shell. Protoconch (Figures 5-7)

with one rounded whorl, maximum diameter 260 pm,

usually heavily eroded, surface sculpture an irregular

network of low ridges. Protoconch and first teleoconch

whorl with coiling axis parallel to final aperture. Suture

deep. First 1.2 teleoconch whorls rounded, sculptured

with weak axial threads; subsequent teleoconch whorls

rapidly expanding, surface sculpture of radial ribs cross¬

ing by thin, curved concentric threads, the two forming

sharp nodules on intersections (Figure 4). Radial ribs

of varying strengths, primary ones thick, raised, 7-8 in

number, each interspace of two adjacent primary ribs

with 2-3 secondary ribs. Outline of aperture elongate-

oval to nearly rounded, aligned on a single plane or

gently arched from side to side. Margin of aperture very

thin and fragile, extending into short digitations that

correspond to primary radial ribs. Periostracum forming

lamellar processes that correspond to intersections of

radial ribs and concentric threads.

Operculum (Figures 2, 24): Very thin, transparent,

attached vertically to posterior region of foot, multispiral,

with large, wide final whorl, margin frayed.

External Anatomy (Figures 8-25): Neck short, wid¬

ened, dorso-ventrally flattened, ventral side with regu-

larlv spaced transversal furrows, each side with

rounded projection or lobe; males with deep groove on

left lateral side, extending to posterior region of mantle

cavity; females with short groove (Figures 12, 13). Mouth

triangular, perioral area with radial furrows; snout

strongly bilobed apieally and drawn out laterally into

points. Eyes absent. Cephalic tentacles postero-laterally

directed, of equal size in female; left tentacle of male

very enlarged, relatively thin where attached to head,

becoming abruptly thicker distally, about four times as

thick as right tentacle, scroll-like in shape, distal end with

a seminal opening, ventrally with a deep, open sperm

groove that continuous as deep groove on left edge of

neck. Mantle skirt very thin. Pallial margin thickened,

without papillae, its edge with one dorsal notch, about

3 mm deep. Mantle cavity opened anteriorly, deep and

spacious. A pallial vein prominently visible on mantle

skirt, originating in right anterior part of mantle skirt

and extending posteriorly to end of mantle cavity.

Ctenidium enlarged, bipectinate, its large size indicative

of filter-feeding, afferent membrane absent; ef ferent axis

arising at posterior of mantle cavity on left, attached to

floor of mantle cavity by thickened efferent membrane;

gill lamellae elongated and curved, with a blunt pointed

S. Zhang and S. Zhang, 2017

Page 79

Figures 1-7. Shell of Lamellomphalus manusensis new species. 1, 2. Holotype, length 8.8 mm, black triangle refers to operculum.

3. Paratype (with periostracum removed), length 6.6 mm. 4. Sculpture. 5. Earlier whorls, white arrow indicate protoconch/

teleoconeh transition. 6. Protoconch. 7. Net-like sculpture on protoconch.

distal end. Columellar muscle horseshoe-shaped, left

one long and slender, right one short and broad, both

extending anteriorly to middle area of neck. Alimentary

groove, or channel, present between right columellar

muscle and right neck projection. Gonad located on

posterior right, behind right columellar muscle. Pericar¬

dium visible as dark structure posterior to gill; ventricle

small but solid, rich in brownish pigment, attached on

Page SO

THE NAUTILUS, Vol. 131, No. 1

Figures 8-16. Soft parts of Lamellomphalus manusensis new species under light microscope. 8, 9. Ventral view of animal of

female and male, respectively. 10. Dorsal view of animal (with mantle skirt removed). 11. Ventral view of head of female; 12, 13. Left

neck portion, white arrows indicate groove on lateral side of female and male, respectively. 14. Ctenidium. 15. Left tentacle of male.

16. Posterior part of foot showing epipodial tentacles. Abbreviations: ct, ctenidium; dg, digestive gland; go, gonad; h, head; 1cm, left

columellar muscle; rcm, right columellar muscle.

S. Zhang and S. Zhang, 2017

Page 81

Figures 17-25. Soft parts and operculum of Lamellomphalus manusensis new species under SEM. 17-18. Ventral view of animal

of female and male, respectively. 19, 20. Ventral view of the head of female and male, respectively; 21. Right lateral epipodial

tentacles. 22. Enlargement of the epipodial tentacles under higher magnification. 23. Posterior epipodial tentacles. 24. Operculum.

25. Ctenidium.

Page 82

THE NAUTILUS, Vol. 131, No. 1

Figures 26-30. Radula of Larnellomphalus manusensis new species. 26. Dorsal view of the radula. 27. Rachidian and lateral teeth.

28. Fourth lateral tooth. 29, 30. Marginal teeth.

7

Shell length (mm)

Figure 31. Scatter plot of shell length vs. shell width across the size range of 100 specimens of Larnellomphalus manusensis

new species.

S. Zhang and S. Zhang, 2017

Page S3

0 02

100

Nodope Ita subnoda GU98428 1 . 1

Nodopelta subnoda GU984280 1

Peltospira operculata GU984279 1

- Peltospira smaragdma GQ 1 60764 1

40

36

- Rhynchopelta concentrica GU984283 1

- Gigantopelta chessoia KU3 1 2689 1

Gigantopelta chessoia KU3 1 2688 1

100

Peltospiridae

48

— Depressigyra globulus DQ093519 1

Peltospira dehcata AY92393 1 1

33

100

- Cyathermia naticoides AY923926. 1

99

Cyathermia naticoides DQ0935 1 8. 1

IjuneUomphalus manusensis sp. nov.

Depressigyra globulus AY 296825 1

42

82

- Pachydermia laevis AB429222. 1

— Pachydermia laevis GU984266 1

Leptogyropsis inflata AB365258 1

-Melanodrymia aurantiaca GQ 1 60763 1

- Melanodrymia aurantiaca AB429220 1

-leptogyra mflata AB330998 1

Neomphalidae

Peltospiridae

Melanodrymiidae

- Bayerotmchus delicatus KU759008 1 | Out git )lip

Figure 32. Neighbour-joining tree for Neomphalina based on suitable COl sequences from GenBank and this study. Numbers

above branches indicate the bootstrap values.

posterior part of efferent membrane of gill. Foot well

developed, rounded, muscular; anterior edge of foot

with transverse furrow marking opening of pedal

gland. Posterior part of foot encircled by epipodial

ridge; epipodial ridge laterally with 4-6 pairs of short,

cylindrical epipodial tentacles, posteriorly with one pair

of relatively developed ones. Epipodial tentacles becom¬

ing smaller anteriorly (Figures 16, 21-23).

Radula (Figures 26-30): Rbipidoglossate, with formula

(ea. 10)+4+l+4-|-(ca. 10). Rachidian teeth and four

pairs of lateral teeth of similar morphology. Base of

rachidian tooth broad, overhanging moderately long

cusp with smooth cutting edges. First to third lateral

teeth slightly less prominent than rachidian tooth,

innermost bases behind that of adjacent lateral tooth.

Fourth lateral tooth with relatively thinner but

longer cusp, outer cutting edge serrated. Marginal

teeth with long shaft, bearing about 20 long denticles

at distal end.

For parameters of shell and scatter plot of shell width

against shell length, please see respectively Table 1 and

Figure 31 .

Type Locality: A hydrothermal vent area at 3° 43' S,

151°40' E, at depth of 1740 m, Manus Back-Arc Basin.

T>pe Material: Holotype (registration number: MBM

283053, collection number: M045-1) and about

130 paratypes (registration number: MBM 283054,

collection number: M045-2) in MBMCAS. All from tvpe

locality, ROV Faxian dive 33, 12 June, 2015.

Distribution and Habitat: Only known from type

locality, where they were found on black, hard min¬

eral rock.

Etymology: The name of new species refers to its

type locality.

Remarks: Shell surface is covered with a thick olive-

green periostraeum that extends beyond the shell edge

and forms lamellar processes on intersections of radial

ribs and concentric threads. This type of periostraeum

may provide a tighter seal along the shell margin and

thus could prevent animal from eventual adverse envi¬

ronmental effects and/or keep potential predators from

dislodging the shell from its substrate.

There are some variations in the shape of the aperture,

from elongate-oval to nearly rounded, the peristoma

aligned on a single plane or gentlv arched from side to

side. As indicated in Figure 31, the ratios shell width:

shell length are relatively constant in young snails, but

become more variable in adults. We assume that these

variations reflect the shape of substratum to which

animal need to adapt.

Molecular Analyses: One sequence was obtained

for the COI region in Lamellomphalus nianusensis.

The sequence has been deposited in GenBank (Accession

number: KY399885). The length of the COI sequence

is 629 bp. The Neighbor-joining (NJ) tree (Figure 32)

was reconstructed using suitable COI sequences from

GenBank and this study. The alignment of COI had a

total 437 bp. The N[ tree shows that Lamellomphalus

nianusensis falls into Neomphalidae in which, together

with Cijatliemiia naticoides Waren and Bouchet, 1989,

it forms a well-supported clade. With available molec¬

ular data, the analysis of a 437-bp fragment of the

COI gene resulted in 15% pairwise distance between

Lamellomphalus and Cyathermia, whereas the range

among Lamellomphalus and six genera of Peltospiridae is

19-25% (see Table 3). As COI sequences alone cannot

provide sufficient evidence to reflect the familial relation¬

ships within this clade, we refrain from discussing any

phylogenetic relationships herein. The purpose of the

analysis was only to show that Lamellomphalus fell into

Neomphalidae clade. The phylogenetic relationship of

Lamellomphalus and other neomphalines needs to be

resolved in a multigene phylogenetic study in the future.

DISCUSSION

Based on available morphological information of shell

and external anatomy, we placed the new taxon in family

Neomphalidae, which confirmed by molecular evidence.

Neomphalidae has sexual dimorphism in which the left

tentacle in males is modified and serves as a penis,

whereas Peltospiridae do not have distinct copulatory

organs or modifications of the cephalic tentacles (Fretter,

1989; Israelsson, 1998). In family Neomphalidae, shell

shape varies greatly from regularly coiled (Cyathermia,

Lacunoides, Planorbidella and Solutigyra ), to haliotiform

( Lamellomphalus ), to limpet-shaped (. Neomphalus and

Symmetromphalus) . Thus, Lamellomphalus nianusensis

could be considered as a intermediate form in

Neomphalidae. Metapodium with an operculum indi¬

cates an incomplete transformation to a limpet-like

body plan. These taxa evidently are of common origin,

but perhaps underwent a series of divergent evolutionary

steps resulting from adaptive radiation. The similarities

among Lamellomphalus and some peltospirids regarding

shell shape, however, should be considered as resulting

from convergent evolution.

In addition to the divergent shell morphologies, there

is also a wide range of variation in the anatomy among

the genera within Neomphalidae, especially in the

morphology of the left tentacle in male individuals.

Lamellomphalus nianusensis possesses a postero-laterally

oriented, scroll-like left tentacle, with a ventral, open

sperm groove and a large proximal seminal opening. How¬

ever, left tentacles of Cyathermia and Lacunoides are

anterior-laterally directed, have a sausage-shaped distal

end, a closed sperm groove, and two prominent proximal

cirri; that of Neomphalus is posteriorly directed, thick,

attached to the neck, tapering to a pointed distal end,

and with open sperm groove; that of Symmetromphalus

is posteriorly directed, sausage-shaped, with dorsal open

sperm groove. The left tentacles of species Solutigyra

S. Zhang and S. Zhang, 2017

Page 85

and Planorbidella are of equal size in both sexes. The

divergent morphologies in left tentacles may have

resulted from different reproductive strategies in the

adaptive radiations of these different clades to chemo-

synthetic environments. High levels of plasticity in shell

and soft parts morphologies could be one of the reasons

for the successful colonization of hydrothermal vents by

this group of marine gastropods.

ACKNOWLEDGMENTS

This research was supported by the Strategic Priority

Research Program of the Chinese Academy of Sciences

(XDA 11030401, XDA1 102030505). We would like to

express our sincere thanks to the crews of R/V Kexue for

their cooperation during the survey. We also thank

Dr. Anders Waren and an anonymous reviewer for their

constructive comments. Special thanks to Dr. Jose H.

Leal for his meticulous editing that led to great

improvements in the manuscript.

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THE NAUTILUS 131(l):87-96, 2017

Page S7

A remarkable infestation of epibionts and endobionts

of an edible chiton (Polyplacophora: Chitonidae)

from the Mexican tropical Pacific

Laura Regina Alvarez-Cerrillo1

Faeultad de Ciencias

Universidad Naeional Autonoma de Mexico

Ciudad de Mexico, MEXICO

Paul Valentich-Scott

Santa Barbara Museum of Natural History

Santa Barbara, CA 93105 USA

William A. Newman

Scripps Institution of Oceanography-

La Jolla, CA 92093 USA

ABSTRACT

Although epibiosis is common in polyplacophorans, we describe

an unusual presence of epibionts and endobionts in a single

adult specimen of Chiton articulatus collected in Guerrero,

Mexico, from an eroded habitat of crevices with high wave

activity. The epibiont and endobiont specimens covered

nearly 90% of the central and lateral areas of the chiton valves

while the border of mantle girdle showed no epibiosis. Crustose

and filamentous algae, and crustacean arthropods from two

common barnacle families, Chthamalidae and Balanidae, rep¬

resent the observed epibionts. Polychaete (Annelida), bivalve

mollusks from two families: Pteriidae (Pinctada mazatlanica )

and Mytilidae (Leiosolenus aristatus), and crustacean arthro¬

pods from the burrowing barnacle family Cryptophialidae

( Cryptophialus wainwrighti) represent the observed endobionts.

In addition, finding of Cryptophialus wainwrighti represents a

new geographic range extension from the type locality in Sinaloa

to Guerrero. Epibiosis studies of invertebrates in the intertidal

rocky shore, such as the dominant C. articulatus, can assist in

understanding ecological relationships and patterns of diversity

in coastal communities.

Additional Keywords: epibiosis, endobiosis, basibiont, Cirripedia,

Chthamalus spp., Balanidae, Polychaeta, Bivalvia, Leiosolenus

aristatus, Pinctada mazatlanica, Acrothoracica, Cryptophialus

wainwrighti

INTRODUCTION

Common in aquatic habitats, epibiosis is the association

between a living substrate organism (basibiont) and a

sessile organism ( epibiont ) attached to the basibionts

outer surface without trophically depending on it (Wahl,

2010). In endobiosis, an organism ( endobiont ) lives under

the external surface of its basibiont (Wahl, 1989, 1997;

Wahl and Mark, 1999; Trigui El-Menif et al., 2008; Wahl,

1 Author for correspondence: [email protected]; Present

address: Faeultad de Ciencias del Mar, Universidad Autonoma

de Sinaloa, Mazatlan, Sinaloa, Mexico.

2010; see Taylor and Wilson, 2002 for a more complex

terminology). In some studies epibiosis is included gen¬

erally as fouling (e.g., Mendez et ah, 2014), biofouling

(e.g., El Ayari et ah, 2015), or without specific terminol¬

ogy (e.g., Buschbaum et ah 2007).

Epibiosis is found worldwide, especially in marine

environments, where any exposed solid surface is likely

to be colonized by organisms (Wahl, 1989). Sessile

organisms are the major constituents of these communi¬

ties (Canning-Clode and Wahl, 2010; Mendez et ah,

2014). The basibionts more frequently studied are mol¬

lusks (Wahl and Mark, 1999; Wahl, 2010), especially those

with economic importance such as gastropods and

bivalves (e.g., see Table 19.2 in Durr and Watson, 2010).

Epibiosis has been poorly documented for the class

Polyplacophora, where epibionts and endobionts occur

in/on the chiton valves. Arey and Crazier (1919) reported

adventitious organisms on the dorsal surface of Chiton

tuberculatus Linnaeus, 1 758, including epizoic barnacles

and algae, with other organisms living between the algae.

Reports of chiton epibiosis have also been represented by

pictures, such as in MacGinitie and MacGinitie (1968:

388, fig. 243) where Mopalia hindsii is pictured with its

valves covered by algae and invertebrates. Bullock and

Boss (1971) documented epibiotic calcareous algae,

bryozoans, polychaete tubes, and the detrimental

endobiont Leiosolenus aristatus (Dillwyn, 1817) boring

into the valves of Chiton stokesii Broderip, 1832, in

the southernmost part of the Panamic Province, and

C. tuberculatus, from the Caribbean. Watters (1981)

reported another eastern Pacific mytilid, Leiosolenus

spatiosa Carpenter, 1857, in the valves of the chiton,

Acanthochitona hirudiniformis (Sowerby I, 1832). Other

epibionts reported on the valves of Chiton tuberculatus

include species of the sessile barnacle genus Tetraclita

Schumacher, 1817, calcareous tube-dwelling polychaetes,

Spirorbis Daudin, 1800 and Serpula Linnaeus, 1758, and

green algae including Ulva Linnaeus, 1753. The algae

provide protection for juvenile mollusks, nematodes,

archiannelids, and protozoans. Bullock and Boss (1971)

did not consider any of the reviewed epibionts to be

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THE NAUTILUS, Vol. 131, No. 1

harmful to the host. Phillips (1972) studied the biota

on the intertidal chiton Mopalia muscosa Gould, 1846,

primarily algae and mollusks, and other organisms.

Dell’Angelo and Lagui (1980) mentioned an epizoic

encrusting bryozoan on the valves of Chiton olivaceus

Spengler, 1797. While most chiton epibiont and endo-

biont observations have been made on intertidal and

snbtidal species, Sigwart (2009a) documented epibiont

foraminifers Hyrrokkin sarcophaga Cedhagen 1994 on

Leptochiton arcticus (G. O. Stirs, 1878).

The endemic Mexican chiton Chiton articulatus

Sowerby in Broderip and Sowerby, 1832, is the largest,

most abundant, and dominant chiton of the intertidal

rocky shore (Galeana-Rebolledo et ah, 2014) found along

the tropical Pacific coast. It occurs between the states

of Sinaloa and Oaxaca, 23°N to 15°N (Ferreira, 1983;

Reyes-Gomez and Salcedo-Vargas, 2002; Kaas et ah,

2006; Reyes-Gomez et ah, 2010). Chiton articulatus is

used as food, for fish bait, and targeted as an artisanal

fishery (Garcia-Ibanez et ah, 2013; Flores-Garza et ah,

2012a). It has gained regional importance and economic

interest in the southern Mexican Pacific, where restau¬

rants offer it as a gourmet and aphrodisiac item (Rios-

Jara et ah, 2006; Avila-Poveda and Abadia-Chanona,

pers. observ.). However, it is not currently cultivated

and is unregulated by the government.

The aim of this work is to describe the epibionts and

endobionts found outside and inside of the valves of a

single adult specimen of Chiton articulatus, collected in

the southern portion of its known area of distribution.

MATERIALS AND METHODS

During one of several campaigns to evaluate the bio¬

diversity of mollusks in the intertidal rocky shores

of Guerrero State, Mexico (Galeana-Rebolledo, 2011;

Flores-Garza et ah, 2012b; Galeana-Rebolledo et ah,

2012, 2014), an unusual adult specimen of Chiton

articulatus was observed to be heavily infested with

epibionts and endobionts. The chiton with epibiosis was

collected at Ojo de Agua, Guerrero, Mexico (17.300°N,

101.0526°W) from exposed rocks facing the open ocean,

where human harvesting would be difficult. The speci¬

men and its epibionts were relaxed following protocols

described by Avila-Poveda (2013), fixed with 90% etha¬

nol, and preserved in 70% ethanol. The specimen mea¬

sured 43.4 mm in length and 32.1 mm in width including

the mantle girdle. This corresponds to the adult stage in

the species, according to Avila-Poveda and Abadia-

Chanona (2013). This specimen was deposited at the

Santa Barbara Museum of Natural History (SBMNH),

Santa Barbara, California, USA (SBMNH 235597).

The epi- and endobionts observed were recorded

according to chiton valve number (I— VIII), identified,

and deposited at the SBMNH and the Coleceion

Nacional de Crustaceos (CNCR) at the Institute de

Biologfa of the Universidad Nacional Autonoma de

Mexico (IB-UNAM).

RESULTS

The epibionts and endobionts specimens cover nearly

90% of the central and lateral areas of the chiton valves,

while the border where the valve had contact with the

mantle girdle did not display epibiosis (Figure 1).

Epibionts

The epibionts included two algal morphotypes, one fila¬

mentous and the other erustose. Both tvpes were distrib¬

uted on every chiton valve. Other epibionts were

crustaceans, two distinct barnacles, chthamalines and

balanids (Figures 1, 12-15), with 26 epibionts in total. All

specimens were <4 mm in diameter. The chthamalines

(Chthamalidae) were Chthamalus Ranzani, 1817 species

(Figures 13-14, SBMNH 235604). Also found were

six tubiferous, calcareous balanid bases with pores

(Balanidae) (Figures 16-17, SBMNH 235609).

Endobionts

One individual of a free-living polychaete (Annelida) was

found in chiton valve VIII. The polychaete could not be

identified due to its small size (< 2 mm length) and

damage during dissection. Mytilidae endobionts were

recorded with 68 individuals of Leiosolenus aristatus

(Dillwyn, 1817) (Figures 2-5, SBMNH 235588-235594);

one L. aristatus specimen had perforated the chiton valve,

ending just 1-2 mm short of the dorsal musculature. One

Pinctada rnazatlanica (Hanley, 1856) specimen was inside

the valve and byssally attached to the chiton valve surface;

whereas two P. rnazatlanica (Figures 6-7, SBMNH

235595-235596) specimens were found deep inside the

valves in abandoned boreholes.

Burrowing acrothoracicans (Cryptophialidae) inclu¬

ded 391 Cryptophialus wainwrighti Tomlinson, 1969

(Figures 8-11, SBMNH 235599 and 235605 and CNCR

29987). The chiton valves had many small, more or less

circular holes on the surface, after dissection of the valves,

each hole yielded one Cryptophialus female. No minute

males were observed. Females, about of I mm in length,

were apparently brooding embryos, as an opened speci¬

men released four ovoid embryos of cyprids with imma¬

ture antennules (Figure 1 1). During dissections (n=4)

eggs were observed. The first female had 23 eggs with no

eyes, in the second female had 10 eggs with eyes, the third

15 eggs with eyes (Fig. 11), and the last female had no

eggs. Eggs with more marked eyes represent the cyprid

stage, and during dissections earliest stages with eyes

forming were observed, but not any earlier naupliar stages.

Abundance by Chiton Valve

Epibionts and endobionts were present on all eight

chiton valves, with 495 individual organisms in total, 6%

were epibionts (n=32) and 94% endobionts (n=463)

(Table 1). The anterior region, valve I to III, had fewer

L.R. Alvarez-Cerrillo et al., 2017

Page S9

Figures 1-7. Chiton articulatus. 1. Dorsal view with numerous juvenile barnacles, largely chthamaline barnacles, plus a few

balanid barnacle bases, generally on the eroded valves encrusted and riddled with smaller epibionts. Scale bar = 1 cm. SBMNH

235597. 2. Mytilid bivalve Leiosolenns aristatus boring into valves. Scale bar = 1 mm. 3. Close up of posterior end of L. aristatus in

valves. Scale bar = 500 pm. 4, 5. Right and left lateral views of L. aristatus, specimen length 1 mm. SBMNH 235588. 6, 7. Pteriid

bivalve Pinctada mazatlanica nestling into old boreholes in valves of C. articulatus. Scale bar = 500 pm.

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THE NAUTILUS, Vol. 131, No. 1

Figures 8-1 1. Chiton articulatus. 8. Close up of valves showing boreholes (arrows indicating some) of the acrothoracican barnacle,

Cryptophialus wainwrighti. Scale bar = 1 mm. 9. Close up of some boreholes showing the opercular bars of the female barnacles

(arrows). Scale bar = 500 pm. 10. Fourteen C. wainwrighti females with eggs and developing embrvos in their mantle cavities (dark

"neck " of sac supporting opercular bars seen in Figure 9, extending toward opening of the burrow). Scale bar = 1 mm. 11. Partially

dissected female with four immature cyprid larvae. Scale bar = 1 mm.

epibionts compared with the central and posterior

regions; valve III had the fewest epihiosis (n=34 organ¬

isms) in contrast, valve VIII had the greatest (n=117

organisms) (Figure IS).

DISCUSSION

Epibionts

Chthamalines and Balanids: There is uncertainty

about the identification of the chthamaline aeom-barnacle

epibionts. According to Meyers et al. (2013), there are

potentially three species of Chthanuilus at this latitude.

One is a northern species that is more typical of sheltered

habitats, C. s outhwardomm Pitombo and Burton, 2007

(according to Newman et al. [2016] proposed name

change). The other two are found in wave-exposed habi¬

tats, the northern C. hedgecocki Pitombo and Burton,

2007 and the southern C. panamensis Pilsbry, 1916. How¬

ever, Chan et al. (2016) restricted the latter to south of

15° N (Tehuantepec), whereby there would be but two

species, C. hedgecocki from exposed environments and

C. southwardorum relatively protected ones. While

chances are that the juveniles on this chiton were likely

the former, the later cannot be ruled out.

Balanid Bases: Likewise, the balanid bases observed

could not be specifically identified. The tubiferous calcar¬

eous bases with pores found are typical of balanids

(Newman and Ross, 1976). However, the bases alone can¬

not be identified to subfamily, much less generic level, as

tlie specimens were incomplete and some were likely

immature. Considering the balanids that are recorded for

this area and their characteristics, die bases could be from

any one of three of die four subfamilies present in the

region: Amphibalaninae Pitombo, 2004, Concavinae Zullo,

1992 and Megabalaninae Newman, 1979.

Endobionts

Polychaeta: Galleries of annelids have also been

observed on other chiton species collected along the

L. R. Alvarez-Cerrillo et al., 2017

Page 91

Figures 12-17. Balanomorph cirripeds from Chiton articulatus. 12. Chthamaline barnacle, Chthamalns sp. (arrow) attached to

valve. Scale bar = 500 pm. 13, 14. Juvenile of Chthamalns sp. removed from one valve and photographed from above and below.

Scale bars = 500 pm and 1 mm respectively. 14. Juvenile Chthamalns sp. in ventral view. Scale bar - 1 mm. 15. Balanid barnacles

(arrows) attached to valve. Scale bar = 1 mm. 16. Tubiferous balanid barnacle bases (arrows) on valve II. Scale liar = 500 pm.

17. Balanid basis (arrow) amongst the algal fronds, between valves II and III. Scale bar = 5 mm.

0 20 40 60 80 100 120

Number of organisms

Figure 18. Abundance distribution of epibionts and endobionts by each valve of a single specimen of Chiton articulatus.

Chiton valves: I. anterior; 1 1— VI 1 , intermediates; VIII, posterior.

L.R. Alvarez-Cerrillo et al., 2017

Page 93

coast of Guerrero, including Chiton alholineatus Broderip

arid Sowerbv, 1829, Lepidochitono sp., Chaetopleura

unilineata Leloup, 1954, and Chaetopleura liirida

(Sowerbv, 1832). While they have not been studied here,

representative specimens are deposited at the Coleccion

Nacional de Moluscos (CNMO| at IB-UNAM.

Leiosolenus aristatus: Bullock and Boss (1971) only

found the mytilid bivalve Leiosolenus aristatus in “large

specimens” of Chiton stokesii Broderip in Broderip and

Sowerby, 1832 and C. tuherculatus (Linnaeus, 1758);

these authors did not report the size of chitons. Watters

(1981) found Leiosolenus spatiosus (Carpenter, 1857) in

three chitons of different sizes, all of them seemingly

adults. Some reports found chiton epibionts only on

larger specimens (Bullock and Boss, 1971; Watters,

1981). In the western Atlantic chiton Ceratozona

squalida (C.B. Adams, 1845), body size was unrelated to

percent cover of epibiotie algae on the girdle (Conelly

and Turner, 2009).

Leiosolenus aristatus occurs in warm-temperate to

tropical waters in the eastern Pacific, western Atlantic,

and eastern Atlantic regions (Valentieh-Seott and

Dinesen, 2004; Coan and Valentieh-Seott, 2012). The

species was reported boring in the valves of Chiton stokesii

and Chiton tuherculatus. Leiosolenus aristatus bores into

calcareous substrates, including the shells of large bivalves

(e.g., Spondylus Linnaeus, 1758, Chanui Linnaeus, 1758,

Ostrea Linnaeus, 1758) and gastropods (e.g., Haliotis

Linnaeus, 1758, Patella Linnaeus, 1758, Stromhus

Linnaeus, 1758, and Pleuroploca (P. Fischer, 1884), as

well as corals and rocks (Coan and Valentieh-Seott,

2012). In the collections of the Santa Barbara Museum

of Natural History (SBMNH), L. aristatus is present

in specimens of Astraea Boding, 1798, Cahjptraea

Lamarck, 1799, Chanui, and Lottia Gray, 1833, as well

as dead coral (Valentich- Scott, pers. obs. November

2016). It is usually found in shallow water, although Coan

and Valentich- Scott (2012) reported shells collected as

deep as 300 m. It has recently has been reported from

the Mediterranean Sea, boring into shells of the muricid

gastropod Stramonita haenuistoma (Linnaeus, 1767)

(El Ayari et al., 2015).

Compared to Chiton stokesii and C. tuherculatus (data

in Bullock and Boss, 1971), the single specimen of

C. articulatus presented here had more Leiosolenus

aristatus individuals boring into its valves. It is possible

that this could be due to differences in shell hardness

and susceptibility for fouling and boring among C.

articulatus and its congeners. Alternatively, the valve

erosion experienced by this chiton specimen might have

played a significant role in allowing epibionts to settle.

Watters (1981) observed chiton valve erosion was a pre¬

requisite to mytilid boring, and that the boreholes

involved the destruction of large portions of both the

tegmentum and articulamentum.

Pinctada mazatlanica: This pteriid bivalve is not a

borer, but likely uses empty Leiosolenus holes as a refuge.

Pinctada mazatlanica is a large species, reaching a length

of 150 mm (Coan and Valentieh-Seott, 2012). The bivalves

are likely only using the chiton valves as a temporary

refuge during a juvenile stage. It is unknown what dam¬

age might occur to the chiton, or to the bivalves them¬

selves, as the pteriids continue to grow.

Acrothoracican Barnacles: Cryptophialus wainwrighti

has been reported from western Mexico (Tomlinson,

1969), found in the marine gastropods Vasula speciosa

(Valenciennes, 1832) and Stramonita hiserialis (Blainville,

1832). The only other eastern Pacific species in the genus

is its Southern Hemisphere (mostly Chilean) counterpart,

Cryptophialus rninutus Darwin, 1854, which is known

to occur within the shells of several mollusks, includ¬

ing Chiton magnificus Deshayes, 1827 (Castilla, 2009;

Kolbasov, 2009; Pitombo 2010). Chiton magnificus is

reported to range from Isla San Lorenzo, Peru (12° S)

to Tierra del Fuego (55° S), but how much of this

remarkably wide range the barnacle occupies is

unknown. Another cryptophialid, Australophialus utinomii

Tomlinson, 1969, attacks the giant chiton, Dinoplax

gigas Gmelin, 1791 (Chaetopleuridae), from South

Africa. Not only are these the only cryptophialid

species known to attack chitons, two of them are

attacking species of the same genus, Chiton. While the

known occurrences were noted in Kolbasov (2009), he

dd not mention chitons in his extended discussion of

interactions between acrothoracicans and their hosts.

Furthermore, while Yeh et al. (2005) listed 18 chiton

species known from Taiwan and nearby islands,

one of which is a species of Chiton, none of the

18 acrothoracicans from Taiwan reported by Chan

et al. (2014), including two species of Cryptophialus,

are known to attack chitons.

The only other acrothoracican barnacle known from

the west coast of Mexico is the lithoglyptid Kochlorine

hamata Noll, 1872. While previously known from else¬

where in the world, Tomlinson (1969) reports it from

Acapulco, Guerrero, Mexico, and in the Gulf of Panama.

The burrow opening of this genus differs from that of

Cryptophialus in being slit-like rather than round or oval

and the opercular bars are correspondingly relatively

long and fusiform with the sac rather than being sup¬

ported by an elongate neck. While K. hamata is known

to attack a wide variety of gastropods as well as coral and

at least one balanomorph barnacle, but like most

acrothoracicans, it is not known to attack chitons.

Although brooding females of Cryptophialus

wainwrighti were found, their age is unknown. Utinomi

(1961) reported on the development one acrothoracican

species, Bemdtia purpurea Utinomi, 1957. Based on his

studies, and that most of the females examined were

sexually mature, it could be assumed that the ones in this

study were at least a year old. It is possible that the

minute males were not observed because they were

dislodged during removal of the females from the chiton

valves or were left attached to the burrow (Tomlinson,

1969). It is possible that earlier nauplius stages occurred

Page 94

THE NAUTILUS, Vol. 131, No. 1

before hatching while the embryos were still retained

O J

within the mantle cavity' (Tomlinson, 1969).

Acrothoracican barnacles can be found in large num¬

bers in limestone as well as in basibionts (Kolbasov,

2009). Pitombo (2010) provides good images of the

Chilean gastropod Concholepas concnmepas Bruguiere,

1789 riddled with the burrows of Cryptophialus minutus.

As an example another eryptophialid, Australophialus

melampygos (Bemdt, 1907), is often found infesting the

New Zealand abalone Haliotis iris Gmelin, 1791. In one

case, up to 3350 boring epibionts were recorded in a

single shell. Australophialus melampygos has also been

reported boring into the mussel Pema canaliculus

(Gmelin, 1791). Haliotis iris and P. canaliculus are exten¬

sively harvested as food sources and the aquaeultural

environment does not appear to provide a suitable habi¬

tat for the recruitment of A. melampygos, perhaps

because of the poor larval mobility of this species

(Batham and Tomlinson, 1965; Webber et ah, 2010).

These findings for the distribution of epibionts and

endobionts on their basibiont are similar to those of

Bullock and Boss (1971), who reported that the posterior

edge of the intermediate valves of chitons is usually more

eroded in large individuals and thus provide a better

substrate for newly settling Leiosolenus. Sigwart (2009a)

showed that parasitic forams preferentially settled on the

posterior valve, apparently because the forams are filter-

feeding when they first settle and then transition to a

true parasitic lifestyle later in life. In Sigwart (2009b),

bryozoan parasites on Nierstraszella Sirenko, 1992, had

posterior distribution, but among the gills, in the ventral

side of the chiton. More epibiosis was recorded on

central and posterior region of the chiton (Figure 18).

The bivalves and sessile barnacles on the chiton valves

were juveniles. It is not known if they can reach their

reproductive state in the limited space on the chiton

valve (Bullock and Boss 1971; Watters, 1981). On the

other hand, the epibiotic relationship may have potential

benefits for barnacles, since their reproductive success

relies on the proximity of the mating individuals (Wahl,

1989); the chiton thus may provide a suitable substratum

for mating to happen in a suboptimal environment.

Although epibionts in other cases may compete with

their host for food resources (Wahl, 1989), this does not

seems likely to be happening between Chiton articulatus

and the epibionts and endobionts observed. This species

of chiton is a rock-scraping grazer, whereas the barnacles

and the bivalves feed on plankton (Celis et ah, 2007;

Goan and Valentich-Seott, 2012).

Epibiosis in this case not only is likely to result in a loss

of functional aesthetes (dorsal chiton valve sensory organs

that could have multiple sensory functions, reviewed in

Vendrasco et al., 2008) but the action of hurrowers (prin¬

cipally L. aristatus and C. wainwrighti) likely leads to

greatly weakened valves (Watters, 1981). Valves also func¬

tion as an important dorsal armor (Vendrasco et al., 2008).

The effects of valve weakening on the behavior of chitons

are unknown although it may affect the movement as

well as strength of their valves, impairing their resistance

to physiological stress during high wave exposure.

Chiton defense mechanisms also could be potentially

negatively affected, as has been reported for burrowing

crabs (Mendez et ah, 2014). The epibiosis on chiton

valves could be potentially highly detrimental to its

normal lifestyle.

While the results presented are from a single speci¬

men, these findings are likely not an isolated case (e.g.,

Alvarez-Cerrillo et al. 2014; 2016), at least in this chiton

species. Epibiosis studies in invertebrates that are domi¬

nant and keystone in the intertidal rocky shores as Chiton

articulatus, could help to understand ecological relation¬

ships and patterns of diversity of the coastal community.

Finally, this chiton species could serve as a model in quest

for answers to different biological, ecological, and fisher¬

ies problems involving epi- and endosymbiosis.

AC KN OWLEDG M E NTS

We thank to Lizeth Galeana-Rebolledo for donating the

chiton specimen. The observation and description of the

specimens was performed at the Instituto de Ciencias

del Mar y Linmologia ICMvL, UNAM, in the Martha

Reguero Lab. Several people collaborated in identifying

the endobionts and epibionts (Hans Bertsch, Elizabeth

Mayen-Pena, Alicia Rojas-Ascencio, Henry Chaney, and

Gretchen Lambert) and by taking photographs (Viridiana

Lizardo- Briseno, Ana Isabel Bieler-Antolin, Susana

Guzman-Gomez, and Daniel Geiger). Finally, we thank

to two anonymous reviewers and to Douglas |. Eernisse

who gave excellent feedback that greatly improved an

earlier draft of this manuscript.

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THE NAUTILUS 131(1): 97—1 00, 2017

Page 97

A new species of Parvaplustrum Powell, 1951 (Gastropoda:

Heterobranchia: Aplustridae) from the northeastern Pacific

Angel Valdes

Department of Biological Sciences

California State Polytechnic University

3801 West Temple Avenue

Pomona, C A 91768 USA

Terrence M. Gosliner

Department of Invertebrate Zoology and Geology

California Academy of Sciences

55 Music Concourse Drive, Golden Gate Park

San Francisco, CA 94118 USA

Anders Waren

Department of Invertebrate Zoology

Swedish Museum ol Natural History

Freseativagen 40, Frescati

SF-11418 Stockholm, Sweden

ABSTRACT

A new species of Parvaplustrum from the northeastern Pacific,

recognized in the literature as undescribed, is formally named

herein. This new species is morphologically distinct from the

two other species in the genus, Parvaplustrum tenerum and

P. japonicum, and distinguishable by its shell sculpture. The

new species is found from Oregon to Baja California, typically

associated with chemosynthetie deep-water environments and

organic-rich sediments.

Additional Keywords: taxonomy, systematic^, shell morphology,

chemosynthetie environments

INTRODUCTION

Parvaplustrum Powell, 1951 is a temperate to cold-water

genus of aplustrid heterobranch sea slugs. Only two

species have been described to date, Parvaplustrum

tenerum Powell, 1951, from the Falkland Islands, and

Parv;aplustrum japonicum Chaban and Chernyshev, 2013,

from the Sea of Japan. A third species from the north¬

eastern Pacific has been cited and discussed in the literature

(Cadien, 1995a; Gosliner, 1996; Chaban and Chernyshev,

2013) but never formally named.

In this paper we provide a formal description of this

species based on specimens collected from California

and Oregon. All the specimens are deposited at the Nat¬

ural History Museum of Los Angeles County (LACM),

the Swedish Museum of Natural History (SMNH), the

Department of Invertebrate Zoology and Geology at the

California Academy of Sciences (CASIZ) and the Scripps

Institution of Oceanography Benthic Invertebrate Col¬

lection (SIO).

Family Aplustridae Gray, 1847

Genus Parvaplustrum Powell, 1951

Parvaplustrum Powell, 1951: 180.

Type Species: Parvaplustrum tenerum Powell, 1951.

Falkland Islands, by original designation.

Diagnosis: Shell ovate, globose; sculpture of extremely

fine and dense spiral striations. Body with two extensi¬

ble appendages on each side of headshield; operculum

absent; radula with single petaliform lateral tooth in each

row, gizzard lacking plates.

Parvaplustrum cadieni new species

(Figures 1-6)

Parvaplustrum sp. A. Cadien, 1995: [pages unnumbered],

Parvaplustrum sp. Gosliner, 1996: 173, figs. 2.2C-D

[ as Pa rva mplustru m ] .

Description: Shell to 2 mm, thin, pyriform (Figure 1).

Body whorl slender to very rotund, spire involute, poste¬

rior margin of outer forming raised lip. Aperture

wide, narrowing slightly mid-length. Sculpture typi¬

cally absent, with very fine spiral lines of punctuations

in larger individuals. Shell color transparent to translu¬

cent w'hite. Protoconch located apicallv on the teleconch,

with 1.5 whorls (Figure 6). Animal not examined alive.

Preserved specimens with a bifid posterior appendage

on each side of headshield (Figure 2). Posterior end of

body forming well defined posterior end. Gill plume

unipinnate (Figure 3), located above head (Figure 4).

Penis elongate, simple. Radula with a single row of

petaliform lateral teeth on each side (Figure 5). No jaws

were observed.

Type Material: Holotype LACM 3329, 390 m, RA'

Velero IV, 17 February 1976, 1 shell specimen, 2.3 mm,

from type locality; Paratype CASIZ 216674, off Point

Arguello, California, 345 m depth, Santa Barbara Chan¬

nel Project, Phase I Reconnaissance (Stn. 61), 1 speci¬

men; Paratype SMNH 44660, Hydrate Ridge, off Oregon

(44° 34' N, 125°08' W), 770 m depth, 1999, RA7 Sonne

Cruise 143 (MUC), 2 specimens.

Page 98

THE NAUTILUS, Vol. 131, No. 1

Figures 1-6. Parvapustrum cadieni new species, scanning electron micrographs. 1. Holotype, 2.1 mm (LACM 3329), off Tanner

Bank, California, photo A. Valdes. 2-4. Details of the external anatomy of a specimen from Oregon (SMNH 44660). 2. Ventral view.

3. Gill. 4. Head (3—4, photos A. Waren). 5. Radular teeth of a specimen from Oregon (SMNH 44660), photo A. Waren. 6. Protoconch

of a specimen from NW of San Nicolas Island, California (LACM 1995-181), photo A. Valdes.

A Valdez et al., 2017

Page 99

Type Locality: Off Tanner Bank, California (32° 40.97' N,

119° 14.(41' W) (RA7 Velero IV 17 February 1976).

Other Material Examined: SMNH 44675, Hydrate

Ridge, off Oregon (44°34.20' N, 125°08.83' W), 777 m

depth, 11 Aug 1999, RA' Sonne Cruise 148 (MUC90D),

8 specimens; SMNH 45424, subduetion zone off the

Oregon coast (44°34.19' N, 125°08.82' W), 787 m

depth, RA7 Sonne Cruise 143, 5 specimens; SMNH

45428, subduetion zone off the Oregon coast

(44°34.207 N, 125°08.81' W), 786 m depth, RA7 Sonne

Cruise 143, 2 specimens; SMNH 111716, Hydrate

Ridge, off Oregon (44°34.255' N, 125°09.289' W),

809 m depth, DSV Alvin dive 4629, 1 specimen; SMNH

111919, Hydrate Ridge, Off Oregon (44°34.118' N,

125°09.076' W), 795 m, DSV Alvin dive 4635, 1 specimen;

Hydrate Ridge, off Oregon (44° 40. 173' N, 125°05.899' W),

618 m depth, DSV7 Alvin dive 4631, 1 specimen; SIO,

Hydrate Ridge, off Oregon (44°40.202' N, 12, §05.876' W),

603 m, DSV7 Alvin dive 4632, 1 specimen; LACM 1995-

181, on a whale skeleton, northwest of San Nicolas

Island, California (33°20,35' N, 119°58.85' W), 960 m

depth, 30 Apr 1995, 6 specimens; LACM 152825, on

a whale skeleton, Santa Catalina Basin, California

(33°11.72' N, 118°29.49' W), 1240 m depth, 14 Oct

1999, DSV Alvin dive 3482, 1 specimen.

Geographic Range: Oregon, possibly from Puget

Sound to Bahia Todos los Santos, Baja California

(D. Cadien, pers. comm.); 3-809 in.

Biology: Found in chemosynthetic deep-water envi¬

ronments such as cold seeps and whale falls (present

paper) as well as organic-rich shelf sediments and deeper

portions of bays (D. Cadien, pers. comm.). Specimens

as small as 1.1 mm show mature reproductive cells

on sectioning, and are assumed reproductively mature

(Cadien, 1995).

Etymology: Named in honor of our friend and col¬

league Don Cadien, who first recognized this species

as undescribed.

DISCUSSION

Although tentatively assigned to the family Aplustridae

(=Hydatinidae) bv Cadien (1995), Gosliner (1996) and

Chaban and Chernyshev (2013), the actual phylogenetic

position of Parvaplustrum remains unknown. Powell

(1951) and Marcus and Marcus (1969) suggested that a

new family might be needed for this group. Because of

the low diversity in Parvaplustrum and rarity of all three

species, no material available for molecular work has

been studied to date. Until such material becomes avail¬

able, relationships among the species and placement of

the genus remain tentative. Parvaplustrum cadieni new

species is here assigned to Parvaplustrum based on

the presence of the diagnostic features listed by Chaban

and Chernyshev (2013), including an ovate-globose

1 1 aminoea -like shell without operculum, two extensible

appendages on each side of the head shield, radula with

a pair of petaliform lateral teeth in a row, and the pres¬

ence of jaws but not gizzard plates.

As already discussed by Chaban and Chernyshev

(2013), Parvaplustrum cadieni new species is clearly

distinct from the two other known species of

Parvaplustrum, and the main differences are found in

the shell morphology. Parvaplustrum tenerum has

extremely fine and dense spiral striations, whereas

P. japonicum has irregularly arranged, numerous, and

extremely small pits and P. cadieni has spiral lines of

punctae. There is also considerable disparity in radular

tooth structure among the type species, P. tenerum,

which has hook-shaped teeth apices (Marcus and

Marcus 1969), and the two taxa from the North Pacific,

with rounded apices.

A fourth possible species, described as

Meloscaphander sp. A by Cadien (1995b) has a more

globose shell than P cadieni, and is very similar to

P. japonicum. This undescribed species is typically

found in shallower waters, 30-605 m, from Goleta to

San Diego, California.

ACKNOWLEDGMENTS

Tl le SEM work was conducted at the California State

Polytechnic University SEM laboratory, supported by

the US National Science Foundation (NSF) grant

DM R- 1429674, and the SMNH SEM lab. Lindsey

Groves (LACM) and Liz Kools (CASIZ) assisted with

the curation of specimens and access to the collec¬

tions. AW thanks Dr. Heiko Sahling (Mamin, Bremen)

for specimens from RA7 Sonne cruises 143 and 148

(1999), and Dr. Lisa Levin (SIO, La Jolla, CA) for

participation in the DSV7 Alvin cruise AT 18-10

(2010). AV thanks Don Cadien and Elena Chaban

for comments on the manuscript and providing

unpublished information.

LITERATURE CITED

Cadien, D.B. 1995a. Parvaplustrum sp. A. SCAM IT [Southern

California Association of Marine Invertebrate Taxonomists]

Newsletter 14. Available via: http://scamit.org/taxontools/

toolbox-new/MOLLUSCA/Subphylum%20Conchifera/

Class%20Gastropoda/Subclass%200rthogastropoda/Super

order%20Heterobranchia/Order%20%22Lower%20Hetero

branchia%22/Superfamily%20Acteonoidea/Family%20ApIus

tridafe/Parvaplustrum%20sp%20A/Parvaplustruni%20sp%

20A.pdf

Cadien, D.B. 1995b. Meloscaphander sp. A. SCAMIT [South¬

ern California Association of Marine Invertebrate Taxono¬

mists] Newsletter 14. Availble via: http://scamit.org/tools/

toolbox/Phylum%20Mollusca/Class%20Gastropoda/Family

%20Aplustridae/Parvaplustrum%20sp%20B.pdf

Page 100

THE NAUTILUS, Vol. 131, No. 1

Chaban, E.M. and A.V. Chernyshev. 2013. New and little-known

shell-bearing heterobranch mollusks (Heterobranchia:

Aplustridae and Cephalaspidea) froni the bathyal zone

of the northwestern part of the Sea of Japan. Deep-Sea

Research II 86-87: 156-163.

Gosliner, T.M. 1996. The Opisthobranchia, pp. 161-213. In:

Scott, P.H., J.A. Blake, and A.L. Lissner (eds.) Taxonomic-

atlas of the Santa Maria Basin and western Santa Barbara

Channel, Volume 9, The Mollusca, Part 2, The Gastropoda.

Santa Barbara Museum of Natural History, Santa Barbara,

California, 228 pp.

Marcus, Ev. and Er. Marcus. 1969. Opisthobranchian and

Lamellarian Gastropods Collected by the “Verna”. American

Museum Novitates 2368: 1-33.

Powell, A.W.B. 1951. Antarctic and subantarctic Mollusca:

Pelecypoda and Gastropoda, collected by the ships of the

Discovery Committee during the years 1926-1937. Dis¬

covery Reports 26: 47-196, pis. 5-10.

Wolfgang Grulke. 2016. Nautilus: Beautiful Survivor.

At One Communications, United Kingdom, 224 pp.,

252x297 mm (landscape format), www.nautilus-thebook

.com, ISBN 978-0-9929740-2-2.

Coined in 1834, the term “scientist” at once allowed

people who thought they should he taken seriously to

distance themselves from less exalted “amateurs”. Among

scholars of the natural world, however, this distinction

has seldom seemed meaningful, and never less so than

today, when information belongs to everyone.

A businessman, author and collector extraordinaire,

Wolfgang Gmlke is an amateur in the original sense of

the word: one who loves the study of nature. Many a

professional might nevertheless wish to have half his

dedication, enthusiasm and resources, which together

have produced this unique work.

Within its broad covers an exhaustive review of the

morphology, reproduction, feeding, and ecology of all

the living Nautilus and Allonautilus species is accompa¬

nied by a detailed history of their discovery and study.

Surrounding this core are fascinating vignettes of their

roles in native and Western art and culture, from furthest

antiquity through the Renaissance, all balanced by a gal¬

lery of astonishing Jurassic and Cretaceous specimens

from various collections. Throughout the book, high-

quality photographs, paintings, portraits, and diagrams

place the colorful living animals and their deep blue

world among the people whose lives and dreams they

have influenced.

Science is nevertheless here in plentv; a chart sets out a

revised phylogeny of the entire family, and the accounts of

Nautilus biology and ecology are fully up to date. There is

a strong conservation message too; the point is well made

that, for a multitude of reasons, the Nautiluses today face

perhaps the biggest challenge to their survival in their

half-billion-year history. In that regard, perhaps the most

important aspect of the book is the juxtaposition of

ancient species with their contemporary counterparts.

“Paleontology” is another venerable term, invented —

in 1822 — to draw a dubious distinction between the

vanished “prehistoric world” and that in which we live

today. The two are one and the same, however, and

placing Nautiluses preserved in stone alongside their

nearly identical living descendants illustrates this in

the clearest way. It may just be a happy coincidence

that all Nautiluses have recently been classified under

Appendix II of the CITES treaty, hopefully granting

them some respite.

As in Gnilke’s previous work "Heteromorph: the Rarest

Fossil Ammonites”, a firm vision and rigorous attention to

detail have ensured that there is none of the poor produc¬

tion and lack of judicious editing that often let down

projects of this scale. Every' page is carefully laid out and

many museums would envy the general sense of coher¬

ence that binds together such a broad diversity of images

and facts.

In summary, I can think of no better book to use in

helping people of any age grasp what “science” actually

embodies - a social activity, a way of thinking and above

all a holistic world view that balances equally what

nature is and what people do. This is definitely a book

for the table, not the shelf; opened to any page, it

cannot fail to capture the eye and begin conversations.

Paul Calloinon

Department of Malacology

Academy of Natural Sciences of Drexel University

Philadelphia, PA 19103 USA

[email protected]

THE 2017 R. TUCKER ABBOTT VISITING CURATORSHIP

The Bailey-Matthews National Shell Museum is pleased to invite applications for the 2017 R. Tucker Abbott

Visiting Curatorship.

The Curatorship, established originally in accordance with the wishes of the late Dr. R. Tucker Abbott, Founding

Director of the Shell Museum, is awarded annually to enable malacologists to visit the museum for a period of one

week. Abbott Fellows are expected, by performing collection-based research, to assist with the euration of portions of

the Museum’s collection and to provide one talk for the general public. The Museum collection consists of marine,

freshwater, and terrestrial specimens. The majority of the collection lots have been catalogued through a computerized

database management system; part of the catalogue is already available for searches online at: http://shellmu.senm.

emc2webs.com/collection/ and via iDigBio at http://ipt.idigbio.org/resource?r=bmnsm-shell. The R. Tucker Abbott

Visiting Curatorship is accompanied by a stipend of $1,500.

Interested malacologists are invited to send a copy of their curriculum vitae, a letter detailing their areas of taxonomic

expertise and research objectives, and to provide a tentative subject for their talk. Send materials to:

Dr. |ose II. Leal, Science Director & Curator

The Bailey-Matthews National Shell Museum

P.O. Box 1580

Sanibel, FL 33957 USA

[email protected]

Applications for the 2017 Visiting Curatorship should be sent electronically to the above e-mail address no later than

May 31, 2017, or postmarked by that date if sent by regular mail. The award will be announced by late June 2017.

Questions about the Visiting Curatorship should be sent to the e-mail address above, or by phone at:

(239) 395-2233; fax (239) 395-6706

THE NAUTILUS 131(1):104, 2017

Page 104

The Delaware Museum of Natural History

is happy to announce and host

the 83,d Annual Meeting of the

American Malacological Society

in Newark, Delaware July 16-21, 2017.

Early registration and abstract submission are open and

reduced rates apply until April 30 .

Please register early!

More infonnation about the meeting, including abstract submission,

graduate student travel grants, social events, and the associated iDigBio

supported Mollusk Digitization workshop can be found at:

http://www.delmnh.org/ams20 1 7/

Registration for meeting, housing and meals can be accessed at:

https://www.regpacks.com/reg/templates/build/?g_id= 100110534

We have two great sessions organized: Mollusks in Peril and Cephalopod

Biodiversity, but there is always room for more! If you are interested in planning a

session, please get in touch with Liz Shea at [email protected].

Sponsored in part by the State of

Florida, Department of State,

Division of Cultural Affairs and the

Florida Council on Arts and Culture

CULTURE

BUILDS

FLORIDA

FLORIDA DEPARTMENT o/STATE

DIVISION oFCULTURAl AFFAIRS

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