THE NAUTILUS

QL

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iz

Volume 130, Number 4

December 8, 201 6

ISSN 0028-1344

A quarterly devoted

to malacology.

EDITOR-IN-CHIEF

Dr. Jose H. Leal

The Bailey- Matthews National

Shell Museum

3075 Sanibel-Captiva Road

Sanibel, FL 33957

EDITOR EMERITUS

Dr. M. G. Harasewych

Department of Invertebrate Zoology

National Museum of

Natural History

Smithsonian Institution

Washington, DC 20560

CONSULTING EDITORS

Dr. Rudiger Bieler

Department of Invertebrates

Field Museum of

Natural History

Chicago, IL 60605

Dr. Arthur E. Bogan

North Carolina State Museum of

Natural Sciences

Raleigh, NC 27626

Dr. Philippe Bouehet

Laboratoire de Biologie des

Invertebres Marins et Malacologie

Museum National d’Histoire Naturelle

55, rue Buffon

Paris, 75005 France

Dr. Robert H. Cowie

Center for Conservation Research

and Training

University of Hawaii

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Department of Biology

College of Charleston

Charleston, SC 29424

Dr. Eileen H. Jokinen

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Dr. Douglas S. Jones

Florida Museum of Natural History

University of Florida

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of Biolog}'

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Florida Museum of Natural History

University of Florida

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Dr. Gary Rosenberg

Department of Mollusks

The Academy of Natural Sciences

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Dr. Angel Valdes

Department of Malacology

Natural History Museum

of Los Angeles County

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Dr. Geerat J. Vermeij

Department of Geology

University of California at Davis

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Columbus, OH 43212-1194

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THE0NAUTILUS

Volume 130, Number 4

December 8, 2016

ISSN 0028-1344

CONTENTS

Sarah Leiner The family Pinnidae (Bivalvia) in the Philippine archipelago:

David Combosch observations on its distribution and phylogeography . 137

Don Dumale

Filipina Sotto

Victor Soliman

Gonzalo Giribet

Jeffrey H.R. Goddard Distribution, seasonality, and prey specificity of Flabellina goddardi

Craig Hoover Gosliner, 2010 (Gastropoda: Nudipleura: Aeolidina) . 146

Kennia Morales A multiple microsatellite assay to evaluate the mating behavior of the

Roland Sanchez intensively exploited marine gastropod Concholepas concholepas

Paulina Bruning (Bruguiere, 1789) (Gastropoda: Muricidae) . 153

Leyln Cardenas

Patricio H. Manriquez

Antonio Brante

Kazutaka Amano Ancistrolepidin gastropods (Buccinidae) from the upper Eocene

Anton Oleinik hydrocarbon seep deposits in Hokkaido, northern Japan . 158

G. Thomas Watters Parachondria joyeuse : a peculiar new species of Hispaniolan Annulariidae

(Gastropoda: Littorinoidea) . 164

In Memoriam . 166

Book Review . 168

Author Index

171

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Sanibel, FL 33957 USA

Editor, Dr. Jose II. Leal, address as above.

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not changed during the preceding 12 months.

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THE NAUTILUS 130(4): 137-145, 2016

Page 137

The family Pinnidae (Bivalvia) in the Philippine archipelago:

observations on its distribution and phylogeography

Sarah Leiner1

David Combosch

Museum of Comparative Zoology

Department of Organismic and

Evolutionary Biology

Harvard University

26 Oxford Street

Cambridge, MA 02138 USA

Filipina Sotto

Marine Biology Section

Department of Biology

University of San Carlos

Cebu City PHILIPPINES

Gonzalo Giribet

Museum of Comparative Zoology

Department of Organismic and

Evolutionary Biology

Harvard University, 26 Oxford Street

Cambridge, MA 02138 USA

Don Dumale

National Museum

Manila. PHILIPPINES

Victor Soliman

Bieol University, Tabaeo Campus

Tabaco City, PHILIPPINES

ABSTRACT

The Philippine archipelago, located in the northern apex of the

Coral Triangle, is known for its high diversity and endemism,

both caused by a complex physical setting modelled by the long

tectonic history of the archipelago and by the more recent

Pleistocene sea-level fluctuations. In order to assess the influ¬

ences of the complex Philippines geography on benthic marine

species, we conducted phylogenetic and phylogeographic

analyses on 71 specimens (out 112 originally collected) often

species of Pinnidae, sequencing two mitochondria] and two

nuclear markers. Our results suggest that the Philippines is a

diversity hotspot for pinnids, with all sampling sites hosting

three or more species, but with marked differences in species

composition in each site, indicating that most pinnids have a

patchy distribution. Our data also suggest that most species

exhibit high levels of genetic connectivity even over large geo¬

graphical distances. As previouly suggested, our data also sup¬

port the idea that the nominal taxon Pinna atropurpurea

includes at least 2 cryptic species in the Philippines.

Additional Keywords: pen shell, cryptic species, diversity

hotspot, biogeography

INTRODUCTION

The Coral Triangle is recognized as a global center of

marine species biodiversity (e.g., Hughes et ah, 2002;

Veron et ah, 2009; Carpenter et ah, 2011; Bellwood

et ah, 2012; Briggs and Bowen, 2013), and is thus

relatively well studied from a biological perspective

( reviewed in Hoeksema, 2007). Within the Coral Triangle

1 Author for correspondence: sarahlemer@g. harvard.edu

region, complex marine currents and successive sea level

fluctuations are thought to have given rise to vicariant

barriers promoting genetic divergence among marine

populations (Briggs, 1999a; Briggs, 1999b; Mora et ah,

2003). Located at the intersection of six tectonic plates,

the Coral Triangle lies between the Pacific and Indian

Oceans, encompassing both sides of a major marine bio-

geographical break known as the Sunda Shelf barrier

(Lourie et ah, 2005), which favors genetic divergence

among populations. Finally the very diverse and exten¬

sive habitats found in the region can also be responsible

for its high biodiversity by creating a refuge from extinc¬

tion for various marine species (Wilson and Rosen, 1998;

Bellwood and Meyer, 2009). The Philippine archipelago

is located at the northern apex of the Coral Triangle,

which also encompasses the Indo-Malay region, New

Guinea, and the Solomon Islands (Figure 1), and is espe¬

cially known for its high species diversity and endemism

(Jones and Kennedy, 2008). The complex physical envi¬

ronment of the Philippine archipelago is a result of its

old and convoluted tectonic history (Hall, 2002), recent

changes in coastlines and basin boundaries associated

with Pleistocene sea-level fluctuations (Sathiamurthy

and Voris, 2006), and present-day oceanographic circula¬

tion patterns (e.g., seasonal currents; Han et ah, 2009).

As a result, this region has shown to strongly influence

dispersal and isolation of marine organisms over evolu¬

tionary and ecological timescales and to shape genetic

structure and species distribution (Juinio-Menez et ah,

2003; Ravago-Gotanco and Juinio-Menez, 2004; Lourie,

et ah, 2005; Ravago-Gotanco et ah, 2007; Payo et ah,

2013). However, most phylogeographic studies con¬

ducted in the area focused mainly on single species and

little has been done to simultaneously study multiple taxa

Page 138

THE NAUTILUS, Vol. 130, No. 4

Figure 1. (A) Phylogenetic relationships of Philippine Pinnidae species inferred from the combined maximum likelihood analysis

of four genetic markers (COl 16S rRNA, 18S rRNA and 28S rRNA). Black squares represent nodes supported by both ML and

Bayesian analyses (>90% bootstrap support or >1.0 posterior probability). (B) Map of sampled localities. The total number of species

and of specimens per species is represented as pie charts for each locality.

or higher taxonomic levels (i.e., genera or families, but

see review in Carpenter et ah, 201 1 ).

Members of the family Pinnidae are commercially

important, large fan-shaped bivalves often found buried

in muddy or sandy substrates of mangroves or seagrass

beds, but also embedded in coral heads. Pinnids are

widely distributed in temperate to tropical waters in the

Indo-Pacific, Atlantic, and Mediterranean Sea. Many

species are commonly found in the Philippine archipel¬

ago, where some are popular food items, e.g., Atrina

pectinata (Linnaeus, 1767) and Atrina inflata (Dillwvn,

1817). Pinnids have a considerable amount of meat

(mostly the adductor muscle) and their extraction is not

regulated in the Philippines, causing them to become a

target economic species that can potentially be overfished.

The family contains two currently recognized genera and

55 accepted species (Turner and Rosewater, 1958;

Rosewater, 1961; Schultz and Huber, 2013; Lemer et ah,

2014). At least 15 species are found in the archipelago

(Poppe, 2010; Schultz and Huber, 2013), which renders

the Philippines the region with the highest known pinnid

diversity in the world. A recent phylogenetic analysis

based on four genetic markers (Lemer, et ah, 2014) iden¬

tified cryptic species in several morphospecies known to

display a wide Indo-Pacific distribution, including Pinna

muricata Linnaeus, 1758; P. saccata Linnaeus, 1758,

P atropurpurea G.B. Sowerby I, 1825, Atrina assimilis

(Reeve, 1858), A. exusta (Gmelin, 1791), and A. pectinata

(Linnaeus, 1767). However, no study has focused on the

Philippine pinnid diversity using genetic markers, despite

the fact that the region may host multiple cryptic species.

Within this context, the major goal of this study is to

provide insights into the pinnid species diversity in the

Philippine archipelago and to compare evolutionary and

life history strategies among species.

MATERIALS AND METHODS

Specimens were collected by SL and DC during a field

trip to the Philippines in May 2013. A total of 112

specimens from ten morphospecies were sampled by

snorkelling and SCUBA diving or obtained from fisher¬

men (samples from Panay) in 5 sites in the vicinities of

Puerto Galera (Mindoro), Panay, Cebu, Panglao (Bohol)

and Bicol (Tables 1, 2; Figure 1). For each locality, we

surveyed both a sandy bay and a coral reef area to opti¬

mize habitat and species diversity. In total, three locali¬

ties were surveyed in the Cebu region, four in Puerto

Galera, two in Panglao and three in Bicol (Table 2).

Due to difficult sea conditions, only 18 specimens were

obtained from fishermen at two localities in Panay.

The 112 specimens reported in Table 1 were used to

describe species composition at each site. Molecular

S. Lemer et al., 2016

Page 139

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analyses were conducted on 71 samples out of the

1 12 specimens (Table 2), due to export permit difficul¬

ties with specimens from some locations. The 71 speci¬

mens used for genetic analyses are deposited in the

Malacology collection of the Museum of Comparative

Zoology, with relevant data accessible through MCZbase

(mczbase.rncz.harvard.edu; Table 2). Molecular markers

consisted of two nuclear ribosomal genes: the nearly com¬

plete 18S rRNA (1.7 Kb) and a ea. 2 Kb fragment of 28S

rRNA; and two mitochondrial fragments for 16S rRNA

(510 bp) and cytochrome c oxidase subunit I (650 bp;

hereafter COI). DNA extraction, amplification, sequenc¬

ing, primers, and protocols are as detailed in Lemer et al.

(2014). Sequence data were visualized and edited in

Geneious Pro 5.3.4 (Drummond et al., 2010) and

aligned with muscle (Edgar, 2004) as implemented in

Geneious. All new sequences have been deposited in

GenBank and all new and previously analyzed sequences

(Lemer et al. 2014) are listed in Table 2. Outgroup

sequences were obtained from Bieler et al. (2014).

Maximum likelihood (ML) analyses were conducted

using RAxML v. 7.2.7 (Stamatalds, 2006) on the four

concatenated genes — the goal of these analyses being to

test the membership of individual specimens to a partic¬

ular species, and not for reconstructing the phylogeny of

the familiv Pinnidae, since this has already been done

elsewhere (Lemer et al. 2014). For the ML searches, a

General Time Reversible model with a discrete gamma

distribution of site-rate heterogeneity (GTR + T) was

specified for each individual data partition (i.e., gene).

Nodal support was estimated via 1000 replicates of a

rapid bootstrap algorithm (Stamatakis et al., 2008) using

tlie GTR-GAMMA model, via the Cyberinfrastructure

for Phylogenetic Research (CIPRES) portal (Miller

et al., 2010). Bootstrap resampling frequencies were

thereafter mapped onto the optimal tree from the inde¬

pendent searches.

Bayesian phylogenetic analyses were conducted in

Beast vl.61 (Drummond and Rambaut, 2007) on the

four concatenated genes, under the GTR+ T substitu¬

tion model for each of 18S rRNA, 16S rRNA and COI

and under the HKY + Y model for 28S rRNA, as recom¬

mended by /ModelTest 2 (Darriba et al., 2012). COI

sequences were partitioned into two sets by codon posi¬

tions, separating third positions from the set of first and

second positions. A relaxed uncorrelated lognormal clock

model was inferred for each partition. The Yule specia-

tion model was assumed for the tree prior and the

starting tree was randomly generated. Markov chains

were run for 10,000,000 generations, sampling every

1000th generation, until convergence. Convergence diag¬

nostics were assessed using TRACER vl.5 (Rambaut and

Drummond, 2007). Five independent runs were sub¬

sequently conducted and combined using LogCombiner

(http://beast.bio.ed.ac.uk/LogCombiner). Phylogenetic trees

were summarized as maximum elade credibility trees

(MCCT), with branch lengths in substitutions per site

after a burn-in of 10,000 in Tree Annotator v. 1.6.2. in

the Beast package (http://tree.bio.ed.ac.uk/software/tracer).

Page 140

THE NAUTILUS, Vol. 130, No. 4

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THE NAUTILUS, Vol. 130, No. 4

Sequences of COI and 16S rRNA were collapsed into

haplotypes using DnaSP and treated as alleles for the

subsequent intra-species analyses. The genealogical rela¬

tionships among haplotypes for each species with 4 or

more haplotypes per marker were assessed by construct¬

ing haplotype networks using a median joining algorithm

as implemented in the software NETWORK 4.6.1. 1

(http://www.fluxus-engineering.com). A parsimony algo¬

rithm was subsequently applied to represent the

most parsimonious intraspecific phylogenies (Polzin and

Daneshmand, 2003).

RESULTS AND DISCUSSION

Although Pinnidae is a relatively diverse family, encom¬

passing about 55 accepted species found in all of the

worlds warm oceans, local species diversity is usually

low (Rosewater, 1961). The majority of pinnid species

inhabit sandy bottoms or mudflats in shallow waters,

mangroves or coral reefs (although some deeper species

exist: Rosewater, 1961; Schultz and Huber, 2013). How¬

ever, more than one species rarely occur in die same site.

This contrasts with the Philippines, where in four sam¬

pled regions (Puerto Galera, Cebu, Panglao and Bicol) at

least three different species of pinnids coexist. Although

most sites have a comparable number of species, species

composition varies among sites (based on the 1 12 speci¬

mens reported in Table 1), indicating that pinnid species

tend to have patchy distributions. This was corroborated

by our field observations, which revealed that most spe¬

cies are represented by small clusters of individuals.

A common pattern was found for Pinna muricata,

P. atropurpurea , Atrina pectinata, and A. inflata ; when

these species were present at a site, they were usually the

most abundant, with only a few representatives of one or

more additional species found among them. For exam¬

ple, our sampled site in the Cebu region was dominated

by P. atropurpurea (12 specimens) and P. muricata

(7 specimens), complemented by a few specimens of

other species (1 specimen of P. trigonium, 1 of A. hystrix ,

2 of A. exusta, 3 of A. vex ilium, and 1 of P. saccata;

Table 1). Similarly, the Bicol region was dominated by

A. inflata , A. pectinata , and A. exusta (10, 8, and 8 spec¬

imens, respectively) with only a few representatives of

other species (1 specimen of Pinna sp. , 1 of P. muricata ,

and 1 of P. saccata). A similar pattern of species distribu¬

tion has been previously observed in a study assessing

the biodiversity and distribution of Pinnidae in Malaysia

(Idris et ah, 2008) and might indicate inter-species com¬

petition for habitat and resources in each site and/or

different reproductive strategies (e.g., low larval recruit¬

ment). A broader sampling in the Philippines would

allow confirming this hypothesis by estimating species

richness, evenness, and diversity indices.

The ML analyses of the four concatenated genes

(-lnL=28, 492. 9666) and the Bayesian analysis produced

nearly identical trees (Figure 1). As previously observed

by Lemer et al. (2014), Atrina and Pinna are reciprocally

monophyletic. Within each genus, the relationships

among species match previous findings based on molec¬

ular data including additional species (Lemer et ah,

2014), with A. inflata being the sister species to a group

identified as “A. pectinata” (although A. pectinata has

recently been attributed to the Indian Ocean only

(Schultz and Hnber, 2013). Atrina hystrix (Hanley,

1858) is the sister species to a clade composed of

A. exusta and A. vexillum. Pinna muricata appears as

the sister species to a clade composed of Pinna sp.,

P trigonium and P. atropurpurea. Pinna saccata is the

most basal clade within the represented Pinna , appearing

as sister group to all other represented species — but it

nests within Pinna in more comprehensive pinnid phylog¬

enies (Lemer et al., 2014). All nodes are well supported

with bootstrap support values >90% and posterior proba¬

bility (pp) values of 1.00. Both the ML and Bayesian trees

show a deep split between two main subclades within

P. atropurpurea (Figure 1). Most haplotype networks obtained

for each analyzed species, except for P. atropurpurea,

display a star-like pattern with one main central haplo-

type shared by multiple localities, and numerous unique

haplotypes separated bv one or two mutational steps

(Figure 2). This pattern, commonly found in popula¬

tions that have undergone a recent demographic expan¬

sion, is not as clear for A. inflata due to the small sample

size, and is absent in the well-sampled P. atropurpurea,

which may constitute more than one species (see Lemer

et al., 2014).

None of the networks obtained display clear geo¬

graphical structure among the sampled sites. On the

contrary, in several instances distant localities shared

identical haplotypes (Figure 2; observed for P. muricata,

A. pectinata , A. exusta and A. vexillum). This result tends

to indicate that despite the complex and fragmented

basins of the Philippines, Pinnidae species show high

levels of genetic connectivity. Habitat fragmentation usu¬

ally tends to limit dispersal capacity and thus lowers

connectivity among populations, even for broadcast¬

spawning bivalves with long pelagic larval duration

(PLD) (Benzie et al., 2002; Kenchington et al., 2006;

Lind et al., 2007a; Lind et al., 2007b). However, low or

absent genetic structure has been previously observed in

other pteriomorphian bivalves with a long PLD inhabiting

fragmented habitats. For example, in a study conducted

with hypervariable microsatellite loci, the black-lipped

pearl oyster Pinctada margaritifera showed little indi¬

cation of genetic structure across French Polynesia

(Lemer and Planes, 2014). Very little is known about the

reproductive strategies and the pelagic larval duration of

most pinnid species, with some exceptions for commer¬

cially important species. Most species are believed to be

gonochoristic, to reproduce annually and to produce

larvae with a long planktotrophic phase with trocho-

phore and veliger stages, such as Pinna atropurpurea,

Atrina pectinata, and Atrina maura (Sowerby I,

1835) (Beer and Southgate, 2006; Mendo et al.,

2011). The potentially long PLD of pinnid species

could thus enable the observed high dispersal capacity,

S. Lemer et al., 2016

Page 143

Figure 2. Haplotype networks for species with four or more samples, using COI (above) and IBS rRNA (below). Lines between

haplotypes are proportional to the number of mutational steps, unless indicated by a number.

even in the highly fragmented habitat context of the

Philippine archipelago.

The haplotype networks obtained for P. atropurpurea

for COI and 16S rRNA show unique haplotypes sepa¬

rated by up to 21 mutational steps. Both the phyloge¬

netic and the non star-like haplotype networks observed

for P. atropurpurea support our previous conclusion:

P. atropurpurea is non-monophyletic in the Pacific

Ocean (Lemer et ah, 2014). In addition, at least two

cryptic species exist in the Philippines. Further work

should thus be conducted to unravel the complexity

of this taxon. In fact, P. atropurpurea appears to be

an intricate species complex composed of cryptic spe¬

cies. Since Rosewater’s (1961) taxonomical revision,

P. atropurpurea, which was initially described with

a distribution limited to the Central Pacific Ocean

(Indonesia, Japan, and the Philippines; Winckworth,

1929), was lumped with P. bicolor (from the Red Sea),

P. dolabrata Lamarck, 1819 (from Southwest Australia),

P. menkei Reeve, 1858, and P. rnadida Reeve, 1858 (from

Northeast Australia) into a single species with a wide

Indo-Pacific distribution, under the name P. bicolor.

Recent morphological (Schultz and Huber, 2013) and

molecular (Lemer, et ah, 2014) work reattributed or sup¬

ported the original name for each of the former species

in each region of the Indo-Pacific.

To conclude, in this study we aimed at assessing

the species and genetic diversity of the commercially

Page 144

THE NAUTILUS, Vol. 130, No. 4

important family Pinnidae in the Philippine archipelago,

where pinnids reach their known peak of diversity. For

this purpose we obtained 1 12 specimens, representing 10

of the 15 species known to be present in the region, from

which 71 were genotyped. Our results suggest that the

Philippines is indeed a diversity hotspot for the family

with all sampled sites hosting three or more species but

with marked differences in species composition in each

site (Table l). As previously suggested by Lemer et al.

(2014), it appears that Pinna atropurpurea is a non-

monophyetic species including at least 2 cryptic species

in the Philippines.

ACKNOWLEDGMENTS

We are indebted to Dr. Yirgilio Palpal-Latoe and

Ms. Vivian Ang of the National Museum, Manila, who

greatly facilitated this collaboration, permit acquisitions,

and the organization of the trip to Puerto Galera. We are

very thankful to the Mayor of Puerto Galera, Hubbert

Christopher A. Dolor, and the Municipal Administrator,

Rafael C. Cataquis, for their welcome and their coop¬

eration. Agricultural Technologist Graeita G. Pelino’s

effort to introduce us to local communities, thus

facilitating the collecting in local area, was priceless.

Alexandra Bagarinao, Liezel Cordel Paraboles, and

Dr. Wilfredo Campos’ help in Panay Island collection were

invaluable. We are indebted to Benjamin Pangatungan

and the University of San Carlos for the use of thejr

laboratory, transportation, and diving facilities. We are

thankful to Renan Bobiles and the Bicol University Tabaco

Campus for their warm welcome, which rendered the trip

in Bicol very comfortable and to Ronnel R. Dioneda from

Bicol University for his help on the field. We would like to

acknowledge all the fishermen, local communities, and

boat owners with whom we interacted during this trip and

who kindly offered their help and cooperation, facilitating

our transportation to various sampling sites. The sampling

and export permits were issued by the National Museum

of Manila and the Bureau of Fisheries and Aquatic

Resources in Cebu. Peter Marko, David Reid, and

Rudiger Bieler provided comments on an earlier version

of this paper. The collecting trip was funded by a Putnam

Expedition Grant from the Museum of Comparative

Zoology. SL was financially supported by a grant from the

Bettencourt-Schuller Foundation. This material was

supported by NSF BivAToL Grant #0732903 to GG.

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THE NAUTILUS 130(4):146-152, 2016

Page 146

Distribution, seasonality, and prey specificity of Flabellina

goddardi Gosliner, 2010 (Gastropoda: Nudipleura: Aeolidina)

Jeffrey H. R. Goddard

Marine Science Institute

University of California

Santa Barbara, CA 93106-6150 USA

[email protected]

Craig Hoover

Biological Sciences Department

California State Polytechnic University

Pomona, CA 91768 USA

ABSTRACT

The aeolid nudibranch sea slug Flabellina goddardi Gosliner,

2010 was described from a single specimen found intertidally

at Tarpits Beef, Carpinteria, California, in 2008. Recently, it

has also been found subtidally at Anacapa Island and two sites

off Malibu, California. We sampled for this species at the type

locality intermittently from November 2008 to June 2016 and

here report on its seasonality, microhabitat, and diet. We found

38 total individuals of die aeolid, all from April to Julv, with die

highest number found in May and June. Most specimens were

observed underneath small ledges, on a tangled faunal mat

consisting mainly of arborescent bryozoans and hydroids.

Laboratory feeding trials and examination of nematocysts in the

aeolid cnidosac indicated that F. goddardi was preying on a

Bougainvillia-Fke, filiferan anthomedusan hydroid. Unlike die

type specimen, many individuals of F. goddardi found since

2008, including subtidal specimens, possessed three white lines

on the body and superficially resembled Flabellina trilineata

(O’Donoghue, 1921), with which F. goddardi may form a mim¬

icry complex. Flabellina goddardi is known only from the

northern half of the Southern California Bight, a geographic

distribution unique among Northeastern Pacific nudibranchs.

Additional Keywords: Aeolid, nudibranch, gastropod, geographic

distribution, northeastern Pacific Ocean, Southern California

Bight, seasonality, diet, hydroid, intertidal, subtidal, mimicry

INTRODUCTION

The aeolid nudibranch Flabellina goddardi Gosliner,

2010 was described based on a single specimen collected

in May 2008 from Tarpits Reef (34.3869,-119.5166) in

Carpinteria, California (Figure 1). The type specimen

was found crawling on macroalage in a low intertidal

pool, providing few clues to its prey and preferred micro¬

habitat, but did lay an egg mass in captivity, allowing for

observations of its embryonic development and hatch¬

ing planktotrophic larvae (Gosliner, 2010; Goddard and

Green, 2013). During sampling trips, since 2008, we

have observed additional specimens of F. goddardi at

the type locality, and in April 2014 the junior author

observed the first specimen found outside the type local¬

ity', at 9 m depth in Las Flores Canyon, off Malibu,

California (Goddard and Hoover, 2014) (Figure 1). More

recently, additional specimens have been observed sub¬

tidally at 18 m depth on the south side of West Anacapa

Island, California (King, 2016a, b; D. Klug, personal

communication to JG, 12 May 2016) and at 9 m depth

off Point Dume, Malibu (Hoover 2016) (Figure 1).

Here, we describe the seasonality and microhabitat of

F. goddardi , present evidence that it preys on a filiferan

anthomedusan (athecate) hydroid, and based on our

examination of the above specimens, supplement the

original description of the color pattern of this delicate

and distinctive species. We also discuss a potential

mimicry complex involving F. goddardi.

STUDY SITE AND METHODS

Tarpits Reef is a sedimentary bench cut by shallow chan¬

nels, pocketed with scattered pools, and short under¬

cut ledges (Figure 2; and see images in Goddard and

Hoover, 2014). The bench extends from the low inter¬

tidal into the shallow subtidal and has an intertidal area

of approximately 2800 m2. Landward it is backed by a

sandy beach approximately 65 m wide and behind that a

marine terrace 2 m high fronted bv sandstone rip-rap

and natural outcrops of asphalt (giving the reef its name).

Sand levels on the beach build through the summer and

can partially fill in low spots on the reef, but then decline

in winter, exposing underlying bedrock and cobble.

To assess the seasonality of F. goddardi we searched

tidepools and the undersides of ledges on Tarpits Reef,

counting all individuals we found during 29 total monthly

trips made from November 2008 to June 2016. After

finding numerous specimens under three small ledges

(e.g., Figure 2) near the landward edge of the reef in

May 2011, we included those ledges in all subsequent

sampling. Combining the samples by month across all years

we conducted at least one search in each calendar month.

Most flabellinids feed on Hydrozoa (Thompson 1976;

McDonald and Nvbakken 1997), so we focused on

J.H.R. Goddard and C. Hoover, 2016

Page 147

Figure 1. Map of Southern California Bight, with small

arrows indicating localities where Flabellina goddardi has

been found. Type locality indicated by asterisk (*).

members of this taxon in determining the prey of

F. goddardi. We collected small samples of the organisms

underlying the slugs at Tarpits Reef and isolated the

different species of hydroids found using a dissection

microscope. In a round of preliminary behavioral trials

conducted in May and June 2011, we cut individual

polyps from the four filiferan hydroids observed, and

holding a polyp by its stalk with watch-maker’s forceps,

tested the reaction of individual slugs to contact on the

anterior part of the head and cephalic tentacles by the

polyps of each of these species. In these trials we noted

the reaction of the slugs as repelled (slug quickly turned

away following contact with a polyp), neutral (no obvious

reaction), or attracted and tried to consume. In four

feeding trials conducted separately in May 2011, June

2011, June 2012, and April 2015, we held 1^4 slugs in

250 ml glass dishes with fresh seawater for up to four

days. Small pieces of each of the filiferan hydroids we

Figure 2. Rock ledge at Tarpits Reef, Carpinteria where many Flabellina goddardi (top inset) have been found. Lower inset shows

two F. goddardi (inside red ovals) stranded at low tide on mixed hydrozoan and bryozoan biota underneath the ledge.

Page 148

THE NAUTILUS, Vol. 130, No. 4

had found were placed wi tl i the slugs and checked twice

daily to see which species the slugs associated with

and, as judged bv missing polyps and (or) coenosarc,

appeared to have preyed upon. During these trials we

changed the seawater in the dishes daily and kept the

fragments of the different species of hydroids separated

from each other. Finally, we compared the cnidome of

the hydroid consumed by the slugs in the feeding trials

with the nematocysts in the cnidosacs of two of the slugs.

We did this by making squashes of fresh individual

polyps and individual cnidosacs on microscope slides,

and comparing the tvpes and size of the component

nematocysts using a compound microscope with a cali¬

brated ocular micrometer. Four specimens of F. goddardi

collected in May 201 1 and one in June 2012 were used

in some of the above trials and were deposited in

the Invertebrate Zoology Collection at the California

Academy of Sciences (CAST/ 186806, 186807, 195985).

RESULTS

Seasonality: Including the type specimen, we have

found a total of 39 specimens of F. goddardi at Tarpits

Reef, mainly during the spring (Figure 3). Specimens

were found from April to July, with the highest total

number of individuals hv month observed in May and

June (28 and 7 individuals, respectively). The highest

number of individuals found per sampling trip was 12 in

Figure 3. Seasonality of occurrence of Flabellina goddardi at

Tarpits Reef. Data collected November 2008 to June 2016

combined by season, across all years, and also include the

finding of the type specimen in May 2008 for an overall total

of 30 sampling trips. Bars indicate mean (+ 1 SE) number of

individuals found per monthly sampling trip, with total number

of trips per season shown in parentheses. Winter = January -

March, Spring = April - June, Summer = July - September.

Fall = October - December.

May 2011, followed by 11 in May 2014. However, no

specimens were found in May 2012 and May 2013, and

no specimens were found from August to March in any

of the years sampled. Subtidally, Flabellina goddardi has

been found off Malibu in May (Goddard and Hoover,

2014; Hoover, 2016) and at Anacapa Island in April and

May (King 2016a, h). One specimen of F. goddardi , until

recently identified as F. trilineata (see Discussion), was

found at Anacapa Island in January 2006 (Segal 2011),

indicating the presence of adults subtidally during at

least some winters. Egg-laying has been observed in the

field and lab in April and May.

Microhabitat and Prey Specificity: All specimens of

F. goddardi found at Tarpits Reef since discovery of the

type specimen were found underneath overhanging

ledges (Figure 2) on a tangled mat consisting of erect

bryozoans and hydrozoans, as well as a tubular cal¬

careous sponge, the stoloniferous octoeoral Clavularia

sp., and the slender, sand-encrusted social ascidian

Euherdmania clavifomiis (Ritter, 1903) (Figure 2, lower

inset). When exposed at low tide, F. goddardi appeared

as small, but distinct semi-translucent white and red

blobs on the surface of this mat (Figure 2, lower inset).

Seven species of hydrozoans were isolated out of the

substrate found under F. goddardi. These included two

leptothecate species: Halecium sp. and the diminutive,

epibiotic Calycella syringa (Linnaeus, 1767), and five

species of filiferan Anthoathecata. The latter included

Eudendrium sp., Bougainvillia- like species A and B

(both with a detritus and particle-encrusted perisarc),

one Cordijlophora- like species, and one unidentified

species. Bougainvillia- like species B was the least abun¬

dant of the filiferan hydroids, and we did not observe

it until June 2012.

In the behavioral trials, F. goddardi was repelled

by contact near the mouth with individual polyps of

Eudendrium sp., the Cordijlophora dike species, and the

unidentified filiferan hydroid, and showed no obvious

reaction to Bougainvillia-like species A (as mentioned

above, we had not found Bougainvillia -like species B

when these trials were conducted).

In the feeding trials, F. goddardi crawled onto and

remained and fed only on Bougainvillia -like species B

(Figures 4, 5, 7), which after three days had lost its polyps

and a significant amount of coenosarc. Additionally, one

specimen of Flabellina goddardi which was isolated with

this species for three days and then held without food for

an additional six days grew from 8.5 mm to 12.5 mm

(total crawling length measured with digital calipers)

and also regenerated a cluster of posterior cerata that

had been missing at the time of collection.

Comparison of the cnidome of Bougainvillia-like spe¬

cies B with F. goddardi cnidosacs (Figure 8) revealed

matching microbasic eurvteles (Figures 6, 9). In addi¬

tion, the hydroid polyps (Figure 5) contained smaller

desmonemes (Figure 6). The microbasic eurvteles from

one cnidosae of a F. goddardi that had been feeding

on Bougainvillia -like species B for 48 hours averaged

J.H.R. Goddard and C. Hoover, 2016

Page 149

Figures 4-9. Hydrozoan prey of Flabellina goddardi. 4. Boug&invillia- like species B. 5. Polyp of Bougainvillia-\iVe species B.

6. Photomicrograph of squash of polyp of BougainvilliaAdke species B with arrows indicating microbasic euryteles. 7. Flabellina

goddardi on Bougainvillia-like species B. 8. Tip of a ceras of F. goddardi, showing cnidosac and subapical red-orange band.

9. Photomicrograph of squash of ceras tip of F. goddardi , with arrows indicating microbasic euryteles.

Page 150

THE NAUTILUS, Vol. 130, No. 4

10.7 jam long (SD = 1.9 pm, n = 16), not significantly

different from those from one polyp of its prey, which

averaged 1 1.9 pm long (SD = 2.0 pm, n = 11) (2 tailed

t-test assuming equal variances, p = 0.13, MS Excel 2013).

We did not observe gonophores or other reproductive

structures on Bougainvillia-\ilm species B. Therefore,

although it resembles Bouaainvillia muscus illustrated

in fig. 40A of Marques et al. (2007), it could be in other

genera of the Bougainvilhidae, or even the Pandeidae,

all of which have cnidomes consisting of mierobasie

eurvteles and desmonemes (P Sehuehert, personal

communication to JG, 20 April 2015). The tentacles of

B ( mga i nvillia-like species B lacked pigment, but the

hypostomes were salmon-colored. The coenosarc of

the hydroid was obscured by the particle-encrusted

perisarc, but did not appear to have much pigmentation

(Figures 4, 5).

Color Pattern: All specimens of F. godclardi found to

date have cerata with bright orange cnidosacs, a sub-

apical red band, and milky to pale olive digestive diver¬

ticula (Figures 2, upper inset; 7, 8). In the specimens

from Anacapa Island, the subapical red band blends into

bright orange which extends halfway or more down each

ceras (Figure 10). The body, head, cephalic tentacles,

rhinophores, and tail are all translucent white. While

the type specimen of F. g oddardi lacked encrusting

white pigment (Gosliner, 2010), many specimens found

since 2008 have possessed broken to relatively complete,

encrusting white lines, one dorsal and medial, running

from the tail to the head, where it bifurcates and con¬

tinues dorsally along each cephalic tentacle, and one

along each side of the body, just below the cerata, which

converge at the tail (Figure 10; Goddard and Hoover,

2014). In some specimens these white lines were incom¬

plete (e.g., see https://www.flickr.eom/photos/34486353@

N07/5744824564), or were represented by mere traces

and fragments. Additionally, some of the subtidal speci¬

mens had a white line running up the posterior side of each

rhinophores (e.g.. Figure 10).

Figures 10-13. Flabellina goddardi and other nudibranchs with similar color patterns found at Anacapa Island, California, spring

2016. 10. Flabellina goddardi. 11. Flabellina trilineata. 12. southern form of Limacia cockerelli. 13. Austraeolis steamsi. .All images

by Douglas King.

[.H.R. Goddard and C. Hoover, 2016

Page 151

DISCUSSION

In the eight years since its discovery, F. goddardi has been

observed at a single intertidal locality and three snhtidal

localities, all in the northern half of the Southern

California Bight (SCB) (Figure 1), which is at the south¬

ern extent of the California Transition Zone, part of the

Oregon Biogeographic Province (Briggs and Bowen, 2012).

A few other Northeastern Pacific nudibranchs appear

to have even more restricted geographic distributions

(e.g., Cuthona hamanni Behrens, 1987 and Eubranchus

sp. 2 of Behrens and Hermosillo (2005), both known only

from La Jolla, California), but none is known solely from

the northern SCB like F. goddardi (see range informa¬

tion in Behrens and Hermosillo, 2005).

Flabellina goddardi appears to specialize on colonies

of a single species of Bougainvillia -like hydrozoan, and,

indeed, the regeneration of cerata and overall growth of

the specimen we held for six days following a bout of

feeding on this hydroid suggests this species is high

quality prey for the aeolid. Other aeolid nudibranchs,

including species of Flabellina, have been previously

recorded feeding on species of Bougairivillia (McDonald

and Nybakken, 1997).

The occurrence of F. goddardi in the spring to early

summer matches that of other small aeolid and dendro-

notacean nudibranchs in California and Oregon (Bertsch

et ah, 1972, Table 5; Nybakken, 1974; personal observa¬

tions) and corresponds with seasonal new growth of many

hydroid species in the region (personal observations).

The three specimens of F. goddardi found at Anacapa

Island in April, 2016 were found in an area of 0.09 m“,

along with two specimens of F. trilineata (Figure 11), and

owing to the similarities in color pattern, were initially

identified as the latter species (D. King, personal commu¬

nication to JG, 1 1 May 2016). Reasoning that F. goddardi

could have been identified as F. trilineata before, we

searched on Google for “ Flabellina trilineata , Anacapa

Island,” and found not only an additional example of the

same misidentification, but that the specimen photographed

had been found more than two years prior to the discovery

of the type specimen of F. goddardi in May 2008 (Segal,

2011). Additional searches for images of F. trilineata from

southern California, including on die Sea Slug Forum

(http://www.seaslugfomm.net/showall/flahtril), Divebums

Species Database (http://speoies.diveburns.eoni/index.phpPD

sciname&n=Flabellina%20trilineata), and Flickr (https://

www.flickr.com/search/?text=flabellina%20trilineata&view_

all = 1 ) did not reveal any more specimens identified as

F. goddardi (nor any additional locality records).

The most obvious external differences between

F. goddardi and F. trilineata are that F. goddardi has

smooth rhinophores, a longer and much more extensible

tail than F. trilineata, and longer cephalic tentacles. These

morphological differences aside, the similarity in color

pattern between the two species is striking, especially at

Anacapa Island, where the subapical red band on the

cerata of F. goddardi grades into orange and extends far¬

ther down the cerata than seen in most specimens from

the mainland (Figure 10). This resemblance raises the

possibility of mimicry between the two species. Two other

nudibranchs found subtidally at Anacapa Island, the

do rid Liniacia cockerelli (MacFarland, 1905) (Figure 12)

and the aeolid Austraeolis steamsi (Cockerell, 1901)

(Figure 13), have dorso-lateral appendages (papillae and

cerata, respectively) similar in color to the cerata of

F. goddardi and F. trilineata, and their rhinophores

are also similar in coloration to those of F. trilineata

(Figure 1 1). Some or all of these four species may form a

Mullerian mimicry complex as a defensive adaptation

against predatory fish.

ACKNOWLEDGMENTS

We thank Peter Schuchert for his assistance in identify¬

ing the nematocysts and hydrozoan prey of Flabellina

goddardi, Liz Kools for her assistance at the California

Academy of Sciences, and Douglas Klug for permission

to use the images in Figure 5. Comments by Hans

Bertsch and an anonymous reviewer improved the

manuscript, and we thank them for their reviews.

LITERATURE CITED

Behrens, D. W. and A. Hermosillo. 2005. Eastern Pacific

nudibranchs. Sea Challengers, Monterey, 137 pp.

Bertsch, H., T. Gosliner, and R. Wharton. 1972. Natural history

and occurrence of opisthobranch gastropods from the

open coast of San Mateo County, California. The Veliger

14: 302-314.

Briggs, J.C. and B.W. Bowen. 2012. A realignment of marine

biogeographic provinces with particular reference to fish

distributions. Journal of Biogeography 39: 12-30.

Goddard, J.H.R. and B. Green. 2013. Developmental mode

in opisthobranch molluscs from the northeast Pacific

Ocean: additional species from southern California and

supplemental data. Bulletin of the Southern California

Academy of Sciences 112: 49-62.

Goddard, J.H.R and C. Hoover. 2014. Flabellina goddardi,

The Slug Site, Opisthobranch of the week (5/12/2014).

Available from: http://slugsite.us/bow2007/nudwk874.htm.

Accessed 7 March 2016.

Gosliner, T.M. 2010. Two new species of nudibranch mollusks

from the coast of California. Proceedings of the California

Academy of Sciences 61: 623-631 .

Hoover, C. 2016. Branching with Ari. [image 1 of 12 is of

F. goddardi] Available from: https://www.facebook.com/

photo. php?fbid= 1 1789661 12136974&set=a. 1 1 789657754

7034 1 . 1 07374 1 840. 1 00000707906493&type=3&theater

Accessed 1 September 2016.

Klug, D. 2016a. Flabellina goddardi Anacapa Island

(nudibranch5Aprl6-16). Available from: https://www

.flickr.eom/photos/8735619@N06/263 1 4263470 Accessed

25 August 2016.

Klug, D. 2016b. Flabellina goddardi Anacapa Island

nudibranch 1 May7-16. Available from: https7Avww.flickr.com/

photos/diverdoug/26390681213 Accessed 26 August 2016.

Marques, A.C., A.E. Migotto, D.R. Calder, and C.E. Mills.

2007. Key to the polypoid stages of Hydrozoa. In: J.T.

Page 152

THE NAUTILUS, Vol. 130, No. 4

Carlton (ed.) The Light and Smith Manual. University of

California Press. Berkeley, pp. 124-137.

McDonald, G.R. and J.W. Nybakken. 1997. A list of the worldwide

food habits of nudibranchs. Available from: http://escholar

ship.org/uc/item/0g75hlq3. Accessed 9 February 2016.

Nybakken, J.W. 1974. A phenology of die smaller dendronotaeean,

arminacean and aeolidacean nudibranchs at Asilomar

State Beach over a twenty-seven month period. The

Veliger 16: 370-373.

Segal, M. 2011. Flabellina goddarcli. Available from: http://www

.carbonos.com/gallery/photo.phpPphoto =907 Accessed

26 August 2016.

Thompson, T.E. 1976. Biology of opisthobranch molluscs,

Vol. I. Bay Society, London, 207 pp.

THE NAUTILUS 130(4):153-157, 2016

Page 153

A multiple microsatellite assay to evaluate the mating behavior

of the intensively exploited marine gastropod Concholepas

concholepas (Bruguiere, 1789) (Gastropoda: Muricidae)

Kennia Morales

Roland Sanchez

Paulina Bruning

Leyla Cardenas 1

Instituto de Ciencias Ambientales y Evolutivas

Facultad de Ciencias, Universidad

Austral de Chile

Isla Teja S/N, Casilla 567

Valdivia, CHILE

Patricio H. Mann'quez

Laboratorio de Eeologfa y Conducta de la

Ontogenia Temprana (LECOT)

Centro de Estudios Avanzados en Zonas Aridas

(CEAZA)

Avenida Ossandon 877

Coquimbo, CHILE

Antonio Brante

Departamento de Eeologfa

Facultad de Ciencias

Universidad Catolica de la

Santfsima Concepcion

Alonso de Ribera, 2850

Concepcion, CHILE

and

Centro de Investigation en

Biodiversidad y Ambientes

Sustentables (CIBAS)

Universidad Catolica de la

Santfsima Concepcion

Concepcion, CHILE

ABSTRACT

The study of reproduction and mating beahavior constitutes a

main issue in biology, ecology and evolution, given its relation

with fitness traits. Here, we developed a simple microsatellite

multiple assay to evaluate the mating strategy and male reproduc¬

tive success of the marine gastropod Concholepas concholepas

(Bruguiere, 1789), an important fishery resource and a key pred¬

ator species of Chilean rocky shore communities. Concholepas

concholepas is a dioecious species with internal fertilization,

encapsulation, and long larval phase. In laboratory, adult males

and females were cultivated in tanks, and 37 larvae from 5 dif¬

ferent clutches were genotyped to run paternity analyses using

seven microsatellite loci. Results showed that promiscuity is

a common mating behavior in C. concholepas displaying an

exceptionally high level of nmltipaternity and males participat¬

ing as fathers in clutches from more than one female. This

microsatellite multiple assay helped to improve our under¬

standing of the reproductive beahavior of this ecological key

species with high economic importance.

INTRODUCTION

Given its importance in determining fitness, studying

reproductive success is crucial to understanding an organ¬

ism’s biology (Stearns, 2000; Avise et aL, 201 1). Also, the

study of the reproductive strategies of commercially

1 Author for correspondence: [email protected]

relevant species is crucial for developing appropriate

conservation and management policies (Defeo and

Castilla, 2005; Hobday et al., 2010). One of the main

challenges in estimating reproductive success in sexual

species is determining an accurate method to quantify

reproductive success; this is especially challenging for

males. Here, we developed a simple multiple microsatel¬

lite assay to study the reproductive strategy and the repro¬

ductive success of the marine gastropod Concholepas

concholepas (Bruguiere, 1789) (Figure 1). Concholepas

concholepas is locally known as “loco” and is one of the

main target species of small-scale artisanal fisheries oper¬

ating along the southeastern coast of Chile (Defeo and

Castilla, 2005). We first tested a set of previously devel¬

oped microsatellite loci for use in paternity analyses. Sec¬

ondly, we inferred some general aspects of the mating

behavior of this species.

MATERIALS AND METHODS

Analyses were run on mature adult individuals obtained

from a single 50 L tank containing an experimental aggre¬

gation of 18 females and 35 males. Individuals were sexed

following methodologies described by Castilla (1974). All

of the reared individuals used in this study were sexually

mature and capable of mating (Manrfquez et al., 2008).

From this experimental aggregation, five clutches laid by

five females identified as potential mothers were studied.

Between five and 1 1 veliger larvae pre-hatching from one

or two ovicapsules were collected at random, and the pater¬

nity of each clutch analyzed. When two ovicapsules were

sampled, larvae from the two capsules were mixed before

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THE NAUTILUS, Vol. 130, No. 4

Figures 1-5. Concholepas concholepas. 1. Group of several individuals (n=l 1 ) laying egg capsules on the rocky shore during low

tide in nothern Chile. 2. Group of three females laying egg capsules on the inside of a glass aquarium. 3. Clutch of newly laid egg

capsules close to the gonadal pore. 4. Newly hatched veliger larvae leaving the apical aperture of a mature egg capsule. 5. Group of

newly hatched larvae 5 min after being released. Abbreviations: Hl-3: female individuals; GP: gonadal pore; NEC: newly laid egg

capsules; NHL: newly hatched larvae.

choosing which would be analyzed. Simultaneously, a

small piece of the muscular foot tissue (less than 1 cm3)

was removed from each adult individual of the experi¬

mental aggregation.

DNA extraction for adults was performed using the

E.Z.N.A.® Tissue DNA kit (OMEGA) following the man¬

ufacturers protocol. To each larva we added 200 pL of 5%

Chelex solution and 2 pL of proteinase K (0.2 mg/mL).

Then, this mixture was incubated at 56°C for 2 hours

followed by 8 minutes at 100°C. A total of 37 veliger

larvae (from 6 ovicapsules) were successfully genotyped.

We selected seven microsatellite loci (Cc2Al 1-1, CclD8,

K. Morales et al., 2016

Page 155

Table 1. Summary statistics of the microsatellite loci used for the paternity analysis of Concholepas concholepas. Locus name,

number of individuals genotyped at the specific locus (N), number of observed alleles (Na), and unbiased expected genetic diversity

(He) are indicated for each locus; adults and larvae were used for calculations. The table shows the probability ol the exact test for

Hardy- Weinberg equilibrium (PHW) and the probability of exclusion (Poxci of 95% confidence level) defined as the probability of

excluding a randomly chosen unrelated candidate parent from the parentage analysis.

Cc21E5, Cc2A5, CelH2, Cc709 and CcQVC) previously

developed to study the spatial population genetics of loco

(Cardenas et al., 2007, 2011). The criteria to select loci

were: (1) level of polymorphism, (2) repeat motif and

(3) amplification pattern. Although amplification patterns

were unambiguous, we checked the microsatellite data for

evidence of null alleles and technical artifacts such as

stuttering and huge allele dropout using MICRO¬

CHECKER 2.2,3 (Van Oosterhout et al., 2004). Genetic

diversity analyses of larvae and adults were performed

using Genetix v. 4.05 (Belkhir et al., 2004). Tests for geno¬

typic linkage disequilibrium and genetic differentiation

were computed using Genepop v. 3.3 (Raymond and

Rousset, 1995).

Paternity analyses as well as estimations of the expected

probability of exclusion of each locus and across loci were

performed using the software CERVUS 2.0 (Marshall et al.,

1998). This procedure employs maximum likelihood

calculations previously proposed by Meagher (1986).

Given the genotypes of the embryos and the known geno¬

type of the mother, paternity was assigned to the male in

the tank with the highest log-likelihood ratio (LOD). In

order to take into account potential misidentifications of

sex, the remaining 53 individuals in the aquarium were

considered as potential fathers. One advantage of using

CERVUS 2.0 is the possibility to evaluate the statistical

significance of the LOD through computer simulations

(here 95% confidence level; Marshall et al., 1998). Com¬

putations were carried out using 10,000 iterations of the

population allelic frequencies estimated using the geno¬

types of the 53 adults studied. We estimated the number

of potential fathers per clutch and whether or not a single

male individual participated in more than one brood. Pos¬

teriorly, we estimated the level of relatedness between all

of the adults (males and females) in the tank using die ML

relate software (Kalinowsld et al., 2006).

RESULTS AND DISCUSSION

Throughout the entire dataset, we found that none of the

loci showed preferential amplification of short alleles or

any evidence of scoring errors or linkage disequilibrium.

All loci were highly polymorphic with 159 alleles

detected in the 53 adults inspected and 112 alleles

detected in the 37 larvae analyzed (Table 1). After

Bonferroni corrections, no significant deviations from

Hardy- Weinberg equilibrium were observed. Altogether,

the probability of exclusion of the seven loci was 0.999,

and the probability of exclusion was high for each of the

seven loci analyzed (Table 1).

From a total of 37 larvae examined, 34 (91.9%) were

unequivocally assigned to only one adult present in the

aquarium. In the remaining cases, analyses could not

discriminate between two males as potential fathers.

The paternity analysis showed that a total of 18 out of

35 males (51.4%) participated in the clutches as fathers

(Table 2). The number of sires per clutch ranged from

three to seven, and the number of fertilized females

per sire ranged from one to three (Table 2); additionally,

sire M19 had the highest percentage of assignments, and

this was achieved with two different female mates

(Table 2). In general, the relatedness analysis indicated

a wide range of kinship between adults in the aquarium.

Most adults were not related (relatedness level = 0).

However, some pairs of individuals were identified

as potential half siblings (relatedness level close to

0.25), and in two cases, some evidence of parental rela¬

tionship was detected (relatedness level close to 0.5).

With the exception of one case in which half siblings

were identified, the potential mates assigned by parent¬

age were not related.

In summary, the seven loci selected here were highly

useful to perform parentage analyses in C. concholepas.

We found evidence of promiscuity and a high level of

multiple paternity in this species which is in concordance

with reports for other gastropod species (Dupont et al.,

2006; Maldnen et al., 2007; Brante et al., 201 1; Xue et al.,

2014). In addition, 94.4% of males that participated as

fathers contributed in more than one brood. From the

information presented here, it wall be possible to design

new experiments using the present multiplex microsatel¬

lite assay to fully understand the mating behavior and

reproductive strategy of C. concholepas.

Page 156

THE NAUTILUS, Vol. 130, No. 4

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ACKNOWLEDGMENTS

LC acknowledges funding from die Millennium Nucleus

Center for supporting the Study of Multiple Drivers of

Marine Soeio-Eeological Systems (MUSELS) via the

MINECON Project NC120086 and Program FONDAP,

Project N° 15150003. The FOND EC YT 1080023 Project

to PHM supported the establishment and maintenance

of the experimental brood-stock. During the writing of

this article PHM was supported by FONDECYT

1130839. AB thanks FONDECYT 1130868.

LITERATURE CITED

Avise, J.C., A. Tatarenkov, and J.X. Liu. 2011. Multiple mating

and clutch size in invertebrate brooders versus pregnant

vertebrates. Proceedings of the National Academy of Sci¬

ences of the United States of America 108: 11512-11517.

Belkhir, K., P. Borsa, L. Chikhi, N. Raufaste, and F. Bonhomme.

2004. GENETIX 4.05, Lxrgiciel sous Windows TM pour la

genetique des populations. Laboratoire genome, popula¬

tions, interactions, CNRS UMR, 5000, 1996-2004. Popula¬

tion genetics software for Windows TM. Universite de

Montpellier 11. Montpellier.

Brante, A., M. Fernandez, and F. Viard. 2011. Microsatellite

evidence for sperm storage and multiple paternity in the

marine gastropod Crepidula coquimbensis . Journal of

Experimental Marine Biology and Ecology 396: 83-88.

Cardenas, L., C. Daguin, J.C. Castilla and F. Viard. 2007.

Isolation and characterization of 1 1 polymorphic micro¬

satellite markers for the marine gastropod Concholmas

concholepas (Brugiere, 1789). Molecular Ecology Notes

7: 464^466.

Cardenas, L., R, Sanchez, D. Gomez, G. Fuenzalida, C.

Gallardo- Escarate and A. Tanguy. 201 1 . Transcriptome anal¬

ysis in Concholepas concholepas (Gastropoda, Muricidae):

Mining and characterization of new genomic and molecular

markers. Marine Genomics, 4: 197-205.

Castilla, J.C. 1974. Notes on mating behaviour of Concholepas

concholepas (Mollusca, Gastropoda, Muricidae) from

Chile. The Veliger 16: 291-292.

Defeo, O. and J.C. Castilla. 2005. More than one bag for the

world fishery crisis and keys for co-management successes

in selected artisanal Latin American shellfisheries. Reviews

in Fish Biology and Fisheries 15: 265-283.

Dupont, L., J. Richard, Y.M. Paulet, G. Tliouzeau, and F.

Viard. 2006. Gregariousness and protandry promote repro¬

ductive insurance in the invasive gastropod Crepidula

fomicata : evidence from assignment of larval paternity.

Molecular Ecology 15: 3009-3021.

Kalinowsld, S.T., A.P Wagner, and M.L. Taper. 2006.

ML-Relate: a computer program for maximum likelihood

estimation of relatedness and relationship. Molecular

Ecology Notes 6: 576-579.

Manrfquez, P.H., A.P. Delgado, M E. Jara, and J.C. Castilla.

2008. Field and laboratory experiments with early ontoge¬

netic stages of Concholepas concholepas. Aquaculture

279: 99-107.

Marshall, T.C., J.B.K.E. Slate, L.E.B. Kruuk and J.M.

Pemberton. 1998. Statistical confidence for likelihood-

based paternity inference in natural populations. Molecular

Ecology 7: 639-655.

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Meagher, T. R. 1986. Analysis of paternity within a natural pop¬

ulation ol Chamaelirium luteum. 1 Identification of most-

likely male parents. American Naturalist 128: 199-215.

Raymond, M. and F. Rousset. 1995. GENEPOP (version 1.2):

population genetics software for exact tests and ecumeni-

cism. Journal of Heredity 86: 248-249.

Stearns, S.C. 2000. Life history evolution: successes, limita¬

tions, and prospects. Naturwissenschaften 87: 476-486.

Van Oosterhout, C., W.E. Hutchinson, D P Wills and P.

Shipley. 2004. MICRO-CHECKER: software for identify¬

ing and correcting genotyping errors in microsatellite

data. Molecular Ecology Notes 4: 535-538.

CV

Xue, D., T. Zhang, and J.X. Liu. 2014. Microsatellite evidence

for high frequency ol multiple paternity in the marine

gastropod Rapana venosa. PLoS ONE 9(1): e86508.

THE NAUTILUS 130(4): 158-163, 2016

Page 158

Ancistrolepidine gastropods (Buccinidae) from the upper Eocene

hydrocarbon seep deposits in Hokkaido, northern Japan

Kazutaka Amano

Department of Geoscience

Joetsu University of Education

1 Yamayashiki

Joetsu 943-8512, JAPAN

[email protected]

Anton Oleinik

Department of Geosciences

Florida Atlantic University

777 Glades Road

Boca Raton, FL 33431 USA

ABSTRACT

Two ancistrolepidine gastropods, Ancistrolepis modestoideus

(Takeda) and Bathyancistrolepis mikasaensis new species are

described from the upper Eocene seep carbonates of the

Poronai Formation in Mikasa City, central Hokkaido. One

specimen of Ancistrolepis sp. resembling A. g rammatus (Dali)

co-occurred with Conchocele bisecta (Conrad) is also described

from the upper Eocene Sakasagawa Formation in Tomamae

Town, northwestern Hokkaido. These species constitute

the oldest to date record of the genera Ancistrolepis and

Bathyancistrolepis. Time of the first appearance of ancistro¬

lepidine gastropods in the North Pacific corresponds with the

increasing number of hydrocarbon seep sites, which could have

affected to accelerated diversification of deep-sea buccinids in

the North Pacific.

Additional Keywords: Eocene, Gastropoda, new species,

Ancistrolepidinae

INTRODUCTION

Most Recent ancistrolepidine gastropods are deep-

shell dwellers and distribution of fossil and modern spe¬

cies is confined to the northern Pacific, except for one

Recent species Ancistrolepis vietnamensis Sirenko and

Goryachev, 1990 from the South China Sea (Tiba

and Kosuge, 1981, 1982; Titova, 1993, 1994; Egorov and

Barsukov, 1994; Higo et al., 1999; Kantor and Sysoev,

2006; Gulbin, 2009). Habe and Sato (1973) origi¬

nally included five genera into the subfamily “Aneistro-

lepisinae”: Ancistrolepis Dali, 1895; Bathyancistrolepis

Habe and Ito, 1968; Clinopegnia Grant and Gale, 1931;

Neancistrolepis Habe and Sato, 1973; and Pseudo-

liomesus Habe and Sato, 1973. However, the generic

composition and status of Ancistrolepidinae remains

somewhat controversial (see Amano et ah, 1996 for

discussion). Moreover, the genus Ancistrolepis was

subdivided into A. eucosmius and A. gramniatus stocks,

based on their size and condition of spiral cords

(Gladenkov et al., 1988; Titova, 1993; Amano et ah, 1996).

In this paper, we adopt the systematic treatment of genera

following Amano et ah (1996).

Genera Ancistrolepis and Bathyancistrolepis first

appeared in the late Eocene and constitute the oldest

record among the subfamily (Titova, 1993). These earli¬

est representatives of the subfamily are important for the

reconstruction of the evolution of the entire subfamily

Ancistrolepidinae. Currently, two species of the genus

Ancistrolepis and one species of the genus Bathyancis¬

trolepis species have been recovered from the upper

Eocene deposits in central and northwestern Hokkaido,

northern Japan. At least one of the Bathyancistrolepis

species is new to science. This article describes these

species and discusses their evolutionary significance.

MATERIALS AND METHODS

Five specimens of Ancistrolepis modestoideus (Takeda,

1953) and two specimens of Bathyancistrolepis mikasaensis

new species were obtained from the seep carbonates

included in mudstones of the upper Eocene Poronai

Formation located at 200 m west of the mouth of

Vayoi Banno Creek, Yayoi Town in Mikasa City, central

Hokkaido (Figure 1, Loc. 1; 43°15'34" N, 141°55'54" E).

The thyasirid Conchocele bisecta (Conrad, 1849), the

vesicomyid Hubertschenckia ezoensis (Yokoyama, 1890),

the carditid Cyclocardia tokudai (Takeda, 1953) were also

recorded by Amano and Jenkins (2007) from the same

locality. One specimen of Ancistrolepis sp. was collected

from the upper Eocene Sakasagawa Formation at the

cliff along the Kotanbetsu River, 2 km west of Seiryu

Bridge in Kiritaehi, Tomamae Town, northwestern

Hokkaido (Figure 1, Loc. 2 = Loc. SK 15 of Noda, 1992;

44°13'22" N,‘ 141°53'8" E) by Mr. Futoshi Akamatsu

(Shunan City, Yamaguchi Prefecture). The same silty

sandstone also contains multiple articulated specimens

of Conchocele bisecta. Abbreviation used is: JUE,

Joetsu University of Education, Joetsu, Niigata Prefec¬

ture, Japan.

K. Amano and A. Oleinik, 2016

Page 159

Figure 1. Locality map of the ancistrolepidine gastropods

examined in this study.

SYSTEMATIC PALEONTOLOGY

Class Gastropoda Cuvier, 1797

Order Neogastropoda Wenz, 1938

Superfamily Buccinoidea Rafinesque, 1815

Family Buecinidae Rafinesque, 1815

Subfamily Ancistrolepidinae Habe and Sato, 1973

Remarks: The subfamily name was originally pro¬

posed as Ancistrolepisinae. This was still used as the

original name by Bouchet and Rocroi (2005), Kantor

and Sysoev (2006) and Gulbin (2009). However, the stem

of the word Ancistrolepis is Ancistrolepid- and should

be correctly used as Ancistrolepidinae (see Goryachev,

1987). Although the paper by Habe and Sato (1972) was

actually published in February, 1973, not in November,

1972 (see Habe, 1973), some authors have mistaken

the date of this publication as 1972 (Gladenkov et ah,

1988; Titova, 1993; Egorov and Barsukov, 1994; Amano

et ah, 1996).

Genus Ancistrolepis Dali, 1895

Type Species: Chrysodomus eucosmius Dali, 1891

Ancistrolepis modestoideus (Takeda, 1953)

(Figures 2-4, 6)

Neptunea nwdestoideci Takeda, 1953: 53-54, pi. 3, 1-7,

pi. 5, fig. 8; Matsui, 1958: 6, pi. 30, figs. la, b; Honda,

1989: 102.

Ancistrolepis modestoideus (Takeda). — Oyama et ah, I960:

60, pi. 8, figs.5a-d.

Ancistrolepis ( Ancistrolepis ) modestoideus (Takeda).—

Titova, 1993: fig. 21.

Material Examined: Among five specimens from the

Poronai Formation, three specimens are deformed (JUE

no. 15941, 15942). All specimens lack early whorls.

Remarks: The type locality of this species was from

the Maoka Group in southwestern Sakhalin, correlated

with the upper Eocene Poronai Formation in Hokkaido

(Takeda, 1953). Titova (1993, p. 4, Fig 21) illustrated one

specimen as A. (A.) modestoideus from the upper Eocene

Takaradai Formation along the Tomari River in south¬

western Sakhalin. Although Oyama et al. (1960) allo¬

cated this species to the genus Ancistrolepis, Honda

(1989) assigned it to the genua Neptunea Roding 1798.

However, when Honda (2000) described a new species

of Ancistrolepis from the lower Oligocene Iwaki Forma¬

tion in Fukushima Prefecture, he mentioned this species

as Ancistrolepis (A.) modestoideus. A Paratype specimen

of A. modestoideus was illustrated from the Yayoi coal

mine near the locality from where we collected the spec¬

imens described herein.

Specimens of A. modestoideus collected by the senior

author are characterized by smaller shells (up to 32.3 mm

in height), four rounded whorls with five to eight spiral

cords on the penultimate whorl and more than ten cords

on body whorl. Spiral cords are prominent, but rounded

and separated by wider interspaces. Overall shape and

details of spiral sculpture are consistent with other authors'

description of this species from Japan and Sakhalin.

Distribution: Upper Eocene Maoka Group and

Takaradai Formation in southwestern Sakhalin, Poronai

Foramtion in central Hokkaido. Lower Oligocene Charo

and Nuibetsu Formations in eastern Hokkaido.

Ancistrolepis sp.

(Figure 5)

Material Examined: One incomplete and deformed

specimen (JUE no. 15943) from the Sakasagawa Forma¬

tion at Kiritachi is examined. The specimen is missing

early whorls.

Description: Shell slightly deformed, moderate in size

(shell height, 53.2 mm+; diameter, 38.6 mm), more than

four whorls. Shoulder angulated with flat area above

shoulder. Shell material mostly dissolved, but surface

sculptured with five prominent spiral cords on penulti¬

mate whorl and more than ten cords on last whorl, sepa¬

rated by wider interspaces.

Remarks: This species resembles the Recent species,

A. grammatus (Dali, 1907) in having a sharply angulated

shoulder, a flat subsutural area above shoulder, similar

number of prominent spiral cords (five to six cords on

penultimate whorl and nine to twelve on body whorl in

A. grammatus-, Okutani, 2000). However, this species is

much smaller than the Recent species. Recent specimen

from off Kurile Islands deposited at JUE attains 128 mm

in shell height.

Page 160

THE NAUTILUS, Vol. 130, No. 4

Figures 2-8. Ancistrolepidine gastropods studied in the paper. 2-4, 6. Ancistrolepis modestoideus (Takeda, 1953).

2, 6. adapertural view, JUE no. 15942, Loc. 1; 3. apertural view, JUE no. 15491. 4. adapertural view of the silicon rubber cast of JUE

no. 15941, Loc. 1. 5. Ancistrolepis sp., adapertural view, |UE no. 15943, Loc. 2. 7, 8. Bathyancistrolepis mikasaensis new species.

7. Holotype, adapertural view, JUE no. 15944, Loc. 1. 8. Paratvpe, adapertural view, JUE no. 15945, Loc. 1.

Ancistrolepis jimgoederti Moore, 1984 from the upper

Oligocene part of the Lincoln Creek Formation in south¬

western Washington is similar to the Kiritachi species in

having a flat subsutural area above the shoulder. How¬

ever, A. jimgoederti differs from Ancistrolepis sp. iu

being larger (up to 70 mm in height) and having fewer

T-shaped spiral cords (only four on penultimate whorl).

Distribution: Upper Eocene Sakasagawa Formation

in northwestern Hokkaido.

Genus Bathyancistrolepis Habe and Ito, 1968

Type Species: Chrysodomus trochoideus Dali, 1907

Remarks: Species in this genus can easily be sepa¬

rated from Ancistrolepis by their small and ovate shell

with low spire. However, some authors treated this genus

as a subgenus of Ancistrolepis (Tiba, 1981; Titova, 1993;

Egorov and Baruskov, 1994). Its representatives live in

deep water (100 to 2000 m; Okutani, 2000) from

Kumano-nada to the southern Kurile Islands (Okutani,

2000; Kantor and Sysoev, 2006).

Bathyancistrolepis mikasaensis new species

(Figures 7, 8)

Diagnosis: A small-sized Bathyancistrolepis species

sculptured with three spiral cords on the penultimate

whorl and eleven on last whorl.

Description: Shell small-sized, attaining 12.5 mm in

height, thin, ovate, with three whorls, protoconch and

juvenile whorls missing. Subsutural groove very narrow

and deep; shoulder rounded. Last whorl is inflated,

occupying approximately 86% of shell height; spire very

low. Surface of penultimate whorl is sculptured with

three sharp spiral cords and separated by very wade

interspaces; last whorl above shoulder with three sharp

cords and base with eight cords separated bv wider

interspaces. Siphonal canal short and rather straight,

without fasciole.

Type Material: Holotype, [UE no. 15944 (Shell

height 12.5 mm + ; diameter 10.0 mm); Paratvpe, JUE

no. 15945 (Shell height 8.0 mm+; diameter 8.3 mm)

Type Locality: The cliff along the Ikushunbetsu River

at 200m west of the mouth of Yayoi Banno Creek, Yayoi

Towm in Mikasa City, central Hokkaido.

Remarks: The new species differs from the Eocene

species, Bathyancistrolepis sitakaraensis (Matsui, 1958)

in having a smaller size (maximum shell height of

B. sitakaraensis, 38 mm), lower spire, and in lacking

interstitial threads between cords.

The Recent species, B. trochoideus (Dali, 1907) can

be easily separated from the new species by its larger

shell (up to 36 mm in height) with some interstitial

threads between main spiral cords and a strongly twisted

siphonal canal.

K. Ainano and A. Oleinik, 2016

Page 161

Etymology: The new species is named for the eitv

from where the type material was collected.

Distribution: Known only from the type locality,

upper Eocene Poronai Formation, Mikasa City, eastern

Hokkaido.

DISCUSSION

The three described species probably lived at or in the

vicinity of methane seeps. In the Poronai site (Loc. 1),

two ancistrolepidine gastropods occurred in the carbonate

indicating relatively low 5n ,JC value (+5.8 to — 44.7%o;

Amano and Jenkins, 2007). Moreover, they are co-occurring

with abundant bivalve species with living counter¬

parts known to host symbiotic chemoautotrophic

bacteria and living at or in the vicinity of methane

seeps, such the thyasirids Conchocele bisecta (Conrad,

1849) and the vesicomyid Hubertschenckia ezoensis

(Yokoyama, 1890). In the Kiritaehi site, although no iso¬

topic data is available, multiple C. bisecta co-occurred

gregariously with Ancistrolepis sp. The occurrence of

Ancistrolepis in association with inferred methane seep-

dwelling mollusks is not unique in the North Pacific.

A North American species, Ancsitrolepis teglandae

(Weaver, 1942) was found in the same assemblage with

the vesicomyid Calyptogena katallaensis (Kiel anti

Amano, 2010) in the lower Oligocene Kulthieth Forma¬

tion in Katalla district, southern Alaska (Kiel and Amano,

2010). These Paleogene occurrences are very' similar to

well-documented Miocene seep sites in Japan. From the

middle Miocene Akanuda Limestone (Bessho Forma¬

tion, Nagano Prefecture, central Honshu), Ancistrolepis

koyamai (Kuroda, 1931) was described by Tanaka

(1959), originally as a species of Buccinum, and was

found co-occurring with Conchocele nipponica (Yabe

and Nomura, 1925), and Adulomya uchimuraensis

Kuroda, 1931. Clinopegma aff borealis Tiba, 1969 has

been recorded from the seep carbonates of the upper

Miocene Morai Formation, co-occurring with Conchocele

bisecta and Calyptogena pacifica Dali, 1891 (Amano,

2003). Very recently, the modem species A. grammatus

has been found from the deep sea (778 m) off the

Paramushir Island, close to the methane seep site with

C. bisecta (Gulbin and Ivin, 2015). Judging from the iso¬

tope record and associated fauna, the Paleogene occur¬

rences of ancistrolepidine gastropods are similar to both

modern and Miocene.

As mentioned above, the genus Ancistrolepis was

subdivided into two stocks: A. eucosmius (Dali, 1891)

and A. grammatus (Dali, 1907) by Titova (1993). More¬

over, two groups were recognized by Titova (1993)

within the A. grammatus stock: A. modestoideus-A.

macneili and A. grammatus groups. The first group is

characterized by a rounded shoulder and absence of the

T-shaped spiral cords while the second group, including

A. grammatus has a flat or concaved area above the

shoulder and T-shaped cords. The oldest known species

of the second group was A. jimgoederti Moore, 1984

from the upper Oligocene part of Lincoln Creek Forma¬

tion (See Titova, 1993). However, Ancistrolepis sp. from

the upper Eocene Sakasagawa Formation at Kiritaehi

belongs to the A. grammatus species group as described

above. Titova (1993) included A. aff. modestoideus as the

oldest species of A. grammatus stock from the upper

Eocene Takaradai Formation in southwestern Sakhalin

into A. modestoideus-A. macneili group. As A. grammatus

group appeared at the same time as A. modestoideus-A.

macneili group, it is possible to separate these groups as

independent stocks.

Titova’s classification of Bathy ancistrolepis is some¬

what confusing. Some of the species should be included

in Ancistrolepis on the basis of their high spire and mod¬

erately inflated last whorl. The following species should

be included in Ancistrolepis grammatus stock: the Oligo¬

cene species, A. chikuzenensis (Nagao, 1928), the Mio¬

cene species, A. togariensis Naruse, 1952 and A. miensis

Araki, 1960. The Miocene species, A. striatus Kanno,

1958 and the Plio-Pleistoeene species, A. masudaensis

Nomura, 1937 should be in the A. eucosmius stock, as

pointed out by Amano et al. (1996). Consequently, the

currently known species of Bathy ancistrolepis include B.

sitakaraensis , B. eguchii (Kamada, 1962), B. trochoideus,

and Bathyancistrolepis mikasaensis new species. As sug¬

gested by Kantor and Sysoev (2006), B. trochoideus

tokoyodaensis Ozaki, 1958 and B. trochoideus ovoideus

(Habe and Ito, 1965) are synonyms of B. trochoideus.

The earliest species of the genus Bathyancistrolepis are

B. sitakaraensis and B. mikasaensis new species from the

upper Eocene formations in Hokkaido.

Buccinid gastropods including the family Ancistro-

lepidinae had rapidly diversified and spread geographi¬

cally within the North Pacific since the late Eocene

(Titova, 1993, 1994). The proposed reason for that

change, traditionally involved climatic deterioration that

started at the end of the Eocene (Titova, 1993). Shallow-

marine gastropods in general were changing stepwise,

from predominantly cosmopolitan to more locally dis¬

tributed tax a (Oleinik and Marincovich, 2003). How cli¬

matic cooling accelerated the diversification and spread

of the Buccinidae remains uncertain. It is at the same

time, during the late Eocene, when Ancistrolepidinae

are found associated with the hydrocarbon seep sites.

The Cenozoic-type seep taxa such as vesicomyids and

bathvmodiolines first appeared in the middle Eocene of

the northern Pacific and significantly expanded their

geographic ranges in the late Eocene (Amano and Kiel,

2007; Amano and Jenkins, 201 1; Kiel and Amano, 2013).

From the middle Eocene onward, the number of seep-

bearing formations suddenly and significantly increased

(Kiel, 2009). The origin of Cenozoic-type seep molluscan

taxa was, therefore, attributed to the increase of a sulfate

concentration in the ocean at the middle Eocene (Kiel,

2015). The ancistrolepidine gastropods examined in this

study have been found in upper Eocene hydrocarbon

seep deposits. Ancistrolepidinae are carnivorous gastro¬

pods and probably fed on the fauna in the seep sites, just

Page 162

THE NAUTILUS, Vol. 130, No. 4

like their modern counterparts do. Recent buccinids such

as Ancistrolepis grammatus, Neptimea spp., Buccinum

spp., Calliloncha spp., Eosipho spp., and Kryptos spp.

have been found in modern seep sites (e.g. Waren and

Bouchet, 2001; Okutani and Lvasaki, 2003; Levin, 2005;

Fujikura et ah, 2008; Fraussen and Sellanes, 2008). As

opportunistic feeders, species from these genera were

also found at modem non-seep localities. In fact, the

majority of the late Eocene and Oligocene occurrences

of Ancistrolepidinae from Kamchatka and Sakhalin are

also from non-seep deposits. The earliest occurrence of

the genera Ancistrolepis and Bathijancistrolepis at the

late Eocene hydrocarbon seep sites suggests that they

adapted seeps as their habitat shortly after their first

appearance in the fossil record. Similar rapid adaptation

for hydrothermal seep habitats were recorded for

serpulid polychates (Vinn et al., 2013). Moreover, mod¬

em species of Ancistrolepidinae are larger than the

Eocene species. Similar trends are observed within

vesicomyids and bathymodiolins (see also Amano and

Kiel, 2007; Kiel and Amano, 2013). These observations

may indicate that the documented late Eocene increase

in the seep sites in the North Pacific and worldwide,

provided ancistrolepidine gastropods with an additional

food resource and helped facilitate their dispersal in the

northern eircum-Pacific.

AC K N O WEE D C M E NTS

We thank Futoshi Akamatsu (Shunan City, Yamaguchi

Prefecture) who kindly offered ancistrilepidin specimen

to KA. We also thank Geerat |. Vermeij (University of

California, Davis) and Steffen Kiel (Swedish Museum of

Natural History) for their useful and constructive

reviews of the manuscript. This study was partly

supported by a Grant-in-aid for Scientific Research

from the Japan Society for Promotion of Science

(C, 26400500, 2014-2016) to KA.

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Yokoyama, M. 1890. Versteinerungen aus der japanischen

Kreide. Palaeontographica 36: 159-202.

THE NAUTILUS 130(4): 164-165, 2016

Page 164

Parachondria joyeuse : a peculiar new species of Hispaniolan

Annulariidae (Gastropoda: Littorinoidea)

G. Thomas Watters

Department of Evolution, Ecology & Organismal Biolog)'

The Ohio State University

1315 Kinnear Road

Columbus, Ohio 43212 USA

watters. 1 @osu.edu

ABSTRACT

Parachondria joyeuse is described from the eastern Dominican

Republic. The new species is characterized by a thin, high-

spired, nearly smooth shell and a peculiar color pattern. It is

placed in Parachondria with reservation.

INTRODUCTION

Bartseh’s 1946 review of the Hispaniolan Annulariidae is

the most comprehensive account of the family thus far

published. However, examination of his sites reveals that

Bartsch and the many collectors from whom he obtained

material had very few collections from the eastern third

of the island. In the 1960s and 1970s, Fred Thompson

and his colleagues from the Florida Museum of Natural

History made numerous collections in these unstudied

areas. The results of these efforts are now being pub¬

lished (Watters, 2013; 2016; and others). They indicate

an unexpected wealth of new taxa and morphological

diversity largely endemic to small areas of the island.

Abbreviations used are: GTW: G. Thomas Watters

collection; UF: Florida museum of Natural History,

Gainesville, Florida.

SYSTEM ATICS

Family Annulariidae Henderson and Bartsch, 1920

Genus Parachondria Dali, 1905

Type Species: Turbo fascia Wood, 1815, by original

designation.

Parachondria joyeuse new species

(Figures 1-7)

Description: Shell thin, fragile, high-spired for family;

spire ca. 3 x the length of aperture. Holotype 14.1 mm

length. Largest adult specimen seen: 16.7 mm length

including lip (paratype 1), smallest 14.1 mm length includ¬

ing lip (holotype). Protoconch wholly or partially lost in

most adults, consisting of 1.5 minute, smooth whorls, not

clearly delimited from teleoconch, white with tan spot on

apex. Teleoconch of ca. 5.75 rounded whorls. Axial sculp¬

ture of teleoconch present only as microscopic, close-set

ridges on first 3-4 whorls, becoming much weaker to

obsolete on remainder of whorls; numerous fine, close-set

growth lines apparent. Spiral sculpture of ca. 30 very

weak, low, subequal, rounded cords. Umbilicus bounded

by weak ridge with smaller cord or ridge within umbilicus.

Suture simple, without tufts or serrations, not channeled.

Aperture teardrop-shaped. Lip single, narrowly expanded,

narrowest facing the umbilicus, weakly auriculate posteri¬

orly, scarcely solute from previous whorl. Color pattern

variable: from white and unpattemed to. boldly patterned.

Pattern of ca. 7 brown, smudged, spiral bands broken

into axially aligned blotches. One band bounds umbilicus,

another broader band may occur within umbilicus. Early

teleoconch whorls usually not banded. Bands persist

over both sides of lip. Operculum paucispiral and corne¬

ous with outer granular, calcareous deposit. Radula and

anatomy unknown.

Type Material: Holotype, UF 216406, 14.1 mm

length; four paratypes, all UF 505262: paratype 1,

16.7 mm length; paratype 2, 15.9 mm length; paratype 3,

15.9 mm length (subadult); paratype 4, 10.6 mm length

(subadult); all from type locality.

Other Material Examined: Total of 35 specimens

distributed as: UF 505263, 19 specimens, including type

material, all from type locality; UF 21641S, one speci¬

men, from type locality; UF 216731, 10 specimens,

13 km NW of Sabana Grande de Boya, Monte Plata

Province; GTW 16522a, five specimens, 321 m elevation,

mesie limestone bluffs behind cemetery. Las Flores

(suburb of Majagual), Monte Plata Province, 19.0397° N,

-69.8390° W.

G.T. Watters, 2016

Page 165

Figures 1-7. Parachondria joyeuse new species. All from type locality. 1, 2. Holotype, UF 216406, 14.1 mm length.

3-6. Paratypes, UF 505262. 3. Paratype 1, 16.7 mm length. 4. Paratype 3, 15.9 mm length. 5-6. Paratype 2, 15.9 mm length.

7. Operculum.

Type Locality: 200 m elevation, 1 km W of Majagual,

Monte Plata Province, Dominican Republic.

Distribution: Known only from the region of

Majagual. This area is in the Sierra tie El Seibo, a

detached portion of the Cordillera Central, in the Los

Haitises Limestone.

Habitat: Specimens have been found at the base of

limestone knolls in mesic vegetated areas and pastures.

None of the specimens were collected alive and only

one still retained an operculum.

Etymology: “joyeuse” (French, joyous) was the sword

of Charlemagne, a reference to the shape and beauty of

the shell and its variability of color. In the IIth century

poem La Chanson de Roland Joyeuse is described as “never

was there a sword to match it; its colour changed thirty

times a day.” “Joyeuse” is used as a noun in apposition.

Remarks: The “polka dot” pattern on a high-spired shell

is shared by several otherwise unrelated and geographi¬

cally distant Hispaniolan annulariids: the Chondropoma

( Wetniorepoma ) complex from the Barahona Peninsula,

Crossepoma emilianum (Weinland, 1S62) from the western

Tiburon Peninsula of Haiti, and particularly Diplopoma

laferrierense ( Bart sell, 1946) from La Ferriere, Haiti, and

Diplopoma elegantissimum (Bartsch, 1946) from Saltrou

(now Belle-Anse), Haiti. All of these substantially differ

from P. joyeuse in sculpture and apertural details, particu¬

larly in the absence of sutural tufts in P. joyeuse. Diplopoma

also differs in having a spiral lamella on the operculum.

The sculpture is somewhat similar to that found in

Samanicola , another veiy unusually sculptured genus,

but the features of the aperture are very different. In

Samanicola the lip is double, widely expanded, and adnate;

in P. joyeuse it is single, narrowly expanded, and solute.

Samanicola is associated with the Samana Peninsula and

P. joyeuse occurs at adjacent Majagual in the Sierra de

El Seibo.

This species is placed in Parachondria with reservation.

That genus (with a Jamaican type species) is currently a

catch-all grouping that undoubtedly contains numerous

distinct phylogenetic groups. Parachondria joyeuse is

similar in its overall sculpture to the Chondropomorus

subgenus of Parachondria. the Hispaniolan members of

which were reviewed by Watters (2016). But the sculpture

of P. joyeuse is microscopic and lacks any evidence of

sutural tufts; the peculiar color pattern does not occur

in other members of Chondropomorus. Further study,

including phylogenetic work, will probably necessitate

the recognition of a separate genus for this species.

AC K N OWLEDGM E NTS

John Slapcinsky (UF) kindly gave me access to that

invaluable collection. The manuscript was significantly

improved by the comments of two anonymous reviewers.

LITERATURE CITED

Bartsch, P. 1946. The operculate land mollusks of the family

Annulariidae of the island of Hispaniola and the Bahama

Archipelago. Bulletin of the U.S. National Museum 192,

264 pp., 38 pis.

Watters, G.T. 2006. The Caribbean land snail family

Annulariidae. Baekhuys Publishers, Leiden, 557 pp.

Watters, G.T. 2013. New taxa and distributional notes on

Ahbottella and related taxa (Gastropoda: Littorinoidea:

Annulariidae). Z ootaxa 3646(1): 1-22.

Watters, G.T. 2016. Review of the Hispaniolan Parachondria

(Chondropomorus) complex (Gastropoda: Littorinoidea:

Annulariidae). Zootaxa 4127(2): 245-275.

William K. Emerson (1925-2016)

William K. Emerson, photo courtesy of AMNH Photo¬

graphic Collection

On October 19, 2016, malacology lost one of its most

respected senior members. William ‘Bill” Emerson died

in New York City at the age of 91, following a 50-year

career mainly spent at the American Museum of Natural

History. It was there that he built a legacy of research,

curation, and public ser\ice, including supervising world-

class exhibitions and serving as President of most of this

country’s major malaeologieal societies. His accolades

include honorary life memberships and other tributes in

recognition of his career achievements.

William Keith Emerson was born in San Diego,

California, on May 1, 1925. He received a Bachelors

degree in zoology from San Diego State University in

1948, followed by a Master’s in zoology from University

of Southern California in 1950, and a Ph.D. in inver¬

tebrate paleontology from University of California at

Berkeley in f 956.

His career at the American Museum of Natural

History began in 1955, when he became Collection

Manager of Quaternary Invertebrates and Assistant

Curator. He was promoted to full Curator in 1966, and

served as Chair of the Department of Living Inver¬

tebrates from 1960 to 1974. During his time at the

Museum, he studied marine gastropods and scaphopods

from the Pacific region, with a focus on systematies and

biogeography. The malacology collection expanded from

74,000 to 275,000 cataloged lots, in which he was assisted

by two exceptional collection managers — William E.

Old, Jr. (at AMNH 1960-1982), and Walter E. Sage III

(1983-1995) — well -respected experts in their own right.

Although Bill often professed that he delegated all shell

club interactions to his collections managers, he fre¬

quently added to their activities personally. For example,

his publications list shows how often he wrote for the

New York Shell Club News; based on their writings about

Bill, he was clearly revered by its members.

Early in his career. Bill participated in extensive expe¬

ditionary work in the Pacific, focusing on mollusean

communities on Pacific Islands that experienced atomic

bomb testing in the early 1950s, such as Bikini Atoll.

In 1957, he led the Puritan-Ameriean Museum of

Natural History Expedition to western Mexico. The

Puritan expedition produced approximately 5,000 lots

of mollusks for the AMNH collection, and resulted in

20 published expedition reports in American Museum

Novitates. Harry Lee, well-known avocational malacolo-

gist from the Jacksonville Shell Club, assisted in curating

the material while a medical school freshman in New

York in 1962. "I was set to work on the shells taken on

the Puritan-Ameriean Expedition (western Mexico),

but I’m not sure I did justice to the task as there were

recurrent distractions such as eonchological conversa¬

tions with the Bills (Old), various other visitors, e.g., Nick

Katsaras (weekly from NJ), Arieh Hadar (Israel), post¬

doctoral fellow Henry Coomans (Netherlands), and

Tucker Abbott, now all likewise free of this mortal coil.

The sessions very often continued into the tearoom of

the Excelsior Hotel, across the street from the northern

rampart of the AMNH, after which we'd all go our sepa¬

rate ways” (H. G. Lee, in litt., 27 October 2016).

Among Bills accomplishments at AMNH was his

documentation of Indo-Pacific mollusks on the eastern

side of the Pacific Ocean. He reasoned that the larvae of

these animals must have dispersed across deep-water

barriers during anomalous warm periods, now known

as El Nino events. Bill also investigated the effects of

oceanic upwelling of cold water on local mollusean pop¬

ulations living along the western coast of North America.

Using these insights about modern biogeography, he

elucidated the distribution of Pleistocene mollusean

communities. He was author or co-author of more than

P. M. Mikkelsen and N.H. Landman, 2016

Page 167

150 research papers on molluscan taxonomy and bio¬

geography (mainly on neogastropods and scaphopods),

and of seven books, notably the popular The American

Museum of Natural History Guide to Shells: Land,

Freshwater, and Marine from Nova Scotia to Florida

(Alfred A. Knopf, 1976), co-authored with Morris “Karl"

Jacobson, a local shell enthusiast.

Bill was an active participant in the creation of quality

exhibitions at AMN'll during bis career. Most notably,

Bill was Chairman of the Planning Committee for

“MoIInsks and Mankind” (later “Mollusks and Our

World,” on display 1975-2000). This exhibit combined

natural history, anthropology, and art, explaining the

habitat and life histories of mollusks as well as their use

bv various cultures.

Bill served malacology as President of the Council of

Systematic Malacologists (1988-1991); President of the

American Malacological Union (1961-1962); President

of the Western Society of Malacologists (WSM; 1968-

1969); Council member of the Society of Systematic

Zoology (1960-1963; 1970-1972); Trustee of the

Delaware Museum of Natural History (1989-1993), and

on many editorial boards. He held research associate

positions at the San Diego Society of Natural History

(1962-1980) and Santa Barbara Museum of Natural

History (1991-2016). Although he spent his career on

the East Coast, his West Coast roots ran deep; "Bill

was part of the “WSM family,” a treasured member of

the malacologists who met annually, supported and

nurtured students and others” (J. Terry Smith, in litt.,

31 October 2016).

As President of the American Malacological Union

(now Society), Bill organized its 28th annual meeting

in 1962 in St. Petersburg, Florida, assisted bv the

O’ 7 J

St. Petersburg Shell Club. Resurrecting his paleonto¬

logical roots, the logo of the meeting included the

Florida Pleistocene gastropod Hijstrivasum horridum

(Heilprin, 1886).

Bill’s many career honors include: Western Society of

Malacologists Award (1972); American Malacological

Union, Honorary Life Member (1987); California Acad¬

emy of Sciences, Honorary Fellow (1987); and Western

Society of Malacologists, Honorary Life Member (1994).

Bill retired in 1995 as Curator Emeritus in the

Department of Invertebrates (later Division of Inverte¬

brate Zoology) after more than 40 years of service. Fol¬

lowing retirement, Bill continued to visit the Museum

daily, to lunch with colleagues, keep up with the literature,

and answer correspondence. He was an avid fan of the

New York Yankees professional baseball team, and could

frequently be seen sporting a Yankees baseball cap. Bill

lost his life partner, Warren Osterwald, in 1995. He is

survived by his brother James Emerson of Colorado

and his nephew Jeffrey Emerson from New York City.

Paula M. Mikkelsen

Integrative Research Center

Field Museum of Natural History

1400 South Lake Shore Drive

Chicago, Illinois 60605, U.S.A.

[email protected]

Neil H. Landman

Division of Paleontology

American Museum of Natural History

Central Park West at 79th Street

New York, New York 10024-5192, U.S.A.

[email protected]

Mans Bertsch and Luis E. Aguilar Rosas. 2016.

Invertebrados Marinos del Noroeste del Mexico -

Marine Invertebrates of Northwest Mexico.

Universidad Autonoma de Baja California, Institute) de

Invetigaciones Oceanologiqas, Ensenada, Mexico, 432 pp.

ISBN 978-0-692-76682-8, $75 (Contact: hansmarvida@

sbcglobal.net) [In English and Spanish.]

Given my lack of familiarity with the region covered in

this bilingual book, I hesitated for a couple of heartbeats

before accepting to review it. However, I was genuinely

curious and thrilled by the concept of an international

cooperation of this type, particularly one involving the

invertebrate fauna of Baja California, the Gulf of California,

and neighboring areas. The senior author, Hans Bertsch,

is a well-known marine biologist and sea-slug specialist

from southern California who lias also published on some

of the cultural aspects of mollusks from the region. Luis

Aguilar Rosas is a respected marine biologist from the

Universidad Autonoma de Baja California in Ensenada.

/^^rgfdciotfor,

Invertebrados Marinos del

Noroeste de Mexico

II am Bertsch & Luis L. Aguilar Rosas

Universidad Autbnoma de Baja California

Institute) de Investigaciones Oceanoldgicas

Knowing previous productions by the authors, I knew

what to expect in terms of choice of subjects and accu¬

racy in their reporting. However, an aspect in particular

stood out during my initial examination of the book, one

that expands the scope of the work into a different realm,

beyond that of a traditional identification guide. The

authors' unique arrangement includes precious cultural

information within the treatment of many species, and in

particular of mollusks. This is not at the expense of accu¬

rate and relevant taxonomic information. The biological

and identification value of the book is augmented by

addition of data on traditional customs of local people,

including uses of some species as food, their spiritual

importance, medicinal and pharmaceutical values, and

others. In many cases, there is also information on the local

nomenclature and the indigenous take on the folk taxon¬

omy of those species. A typical species entry contains

(in addition to the scientific and common names and great

color illustrations) the subsections Description, Size,

Habitat, [geographic] Distribution, and Remarks (cultural

and ethnographic information, when available, is included

in this latter subsection). Entries in the section on mol¬

lusks, in most cases, include an image of the live animal.

The section on Mollusks comprises 390 species, for a total

of 806 species (48 %) treated in the book (hence the

relevance of this review in The Nautilus). There is a glossary

and separate literature sections for the different groups

(the literature section for Mollusca alone spans 7.5 pages).

The volume also includes essays by Jose Luis Carballo,

Donald Potts, Jesus Angel de Leon-Gonzalez, Paul

Valentich-Scott, and Francisco A. Solis-Marin. The indi¬

vidual sections benefitted from the taxonomic expertise

and contributions of a large cadre of international special¬

ists in the different phyla. Spot checks reveal that the

taxonomy and binominal nomenclature is up to the most

recent standards compiled in the World Register of

Marine Species (WoRMS Editorial Board, 2016.)

Did the authors aim to provide a complete guide

of regional marine invertebrates for northwestern

Mexico? They didn’t, but this doesn’t detract from the

usefulness of their production. For instance, from the

standpoint of mollusks, there are gaps in the taxonomic

coverage of the phylum, with lack of a more compre¬

hensive coverage for some families of microgastropods

and small bivalves. It is not a purpose of the book,

however, to include the entire representation of inver¬

tebrates for the covered area, but to present a selection

of the most conspicuous and relevant taxa that fit in a

handy book format.

This production by Bertsch and Aguilar Rosas is

symbolic of a much-desired type of cooperation between

J.H. Leal, 2016

Page 169

the two great North American nations. No dividing wall

separates the complementary interests and important

contributions from these two authors. On the contrary,

there is a clear synergistic component in their work.

Beyond its efficacy as an invertebrate field guide,

Bertsch and Aguilar Rosass stimulating volume tran¬

scends its regional-guide aspect to become a very read¬

able narrative of the taxonomy, natural history, ecology,

and cultural aspects of the species it covers.

LITERATURE CITED

WoRMS Editorial Board. 2016. World Register of Marine

Species. Available from http://www.marinespecies.org at

VLIZ. Accessed 2016-10-22. doi:10. 14284/170

Jose H. Leal

Bailey- Matthews National Shell Museum/The Nautilus

Sanibel, FL 33957 USA

[email protected]

THE0NAUTILUS

Volume 130

2016

Amano, K .

Amaral, V.S .

Bhave, V. .

Brante, A .

Breure, A.S.H. .

Bruning, P. .

Cabrera, F. .

Cardenas, L .

Coan, E.V. .

COMBOSCH, D .

DeVries, T.J .

Dumale, D .

Fields, A .

Garcia, E.F. .

Giribet, G .

Goddard, |.H.R.

Hickman, C.S. ...

Hoover, C .

Hovestadt, A .

Jenkins, B.G .

Kabat, A.R .

Landman, N.H. .

Leal, J.H .

Lemer, S .

AUTHOR INDEX

116,158 Lyons, W.G . 127,134

. 53 Manri'quez, P.H . 153

. 72 Martinez, S . 5

. 153 Medrano, S . 72

. 27 Mikkelsen, PM . 166

. 153 Morales, K . 153

. 5 Norbis, W. . 5

. 153 Oleinik, A. 0 . 116,158

. 17 Portell, R.W. . 13

. 137 Robinson, D.G . 27

. 101 Sanchez, R . 153

. 137 Schmelz, G.W . 13

. 27 Simone, L.R.L . 53

79, 127 Snyder, M.A . 122, 127, 134

. 137 Soliman, V. . 137

. 146 Sotto, F . 137

. 83 Valdes, A . 72

. 146 Vermeij, C.J . 122

. 27 Watters, G.T. . 23, 164

. 116 Wicksten, M.K . 132

. 17 Zhang, | . 1

. 166 Zhang, Sh . 1

. 168 Zhang, Sr . 1

. 137

NEW TAXA PROPOSED IN VOLUME 130

GASTROPODA

Achnete katsurihaensis Amano and Oleinik, 2016, new species (Cancellariidae, fossil) . 1 17

Batlujacmaea lactea Zhang, Zhang, and Zhang, 2016, new species (Pectinodontidae) . 3

Bathyancistrolepis mikasaensis Amano and Oleinik, 2016, new species (Buccinidae, fossil) . 160

Calliotropis andamanensis Hickman, 2016, new species (Calliotropidae) . 88

Calliotropis enantioserrata Hickman, 2016, new species (Calliotropidae) . 86

Calliotropis locolocoensis Hickman, 2016, new species (Calliotropidae) . 93

Calliotropis lumuluensis Hickman, 2016, new species (Calliotropidae) . 94

Calliotropis tabakaensis Hickman, 2016, new species (Calliotropidae) . 92

Calliotropis tominiensis Hickman, 2016, new species (Calliotropidae) . 90

Chondropoma bellavittatum Watters, 2016, new species (Annnlariidae) . 23

Cuthona luciae Valdes, Medrano, and Bhave, 2016 new species (Tergipedidae) . 74

Fasciolaria delicatissima Garcia, Lyons, and Snyder, 2016, new species (Faseiolariidae) . 128

Hesperaptyxis Snyder and Vermeij, 2016, new genus (Faseiolariidae) . 122

Hesperaptyxis negusi Snyder and Vermeij, 2016 (Faseiolariidae) . 124

Misifulgur DeVries, 2016, new genus (Buccinidae, fossil) . 103

Misifulgur dockeryi DeVries, 2016, new genus (Buccinidae, fossil) . 104

Misifulgur macneili DeVries, 2016, new genus (Buccinidae, fossil) . 106

Misifulgur montemarensis DeVries, 2016, new genus (Buccinidae, fossil) . Ill

Parachondria joyeuse Watters, 2016, new species (Annulariidae) . 164

Truncatella andymurrayi Schmelz and Portell, 2016, new species (Truncatellidae, fossil) . 14

Truncatella chipolana Schmelz and Portell, 2016, new species (Truncatellidae, fossil) . 14

Truncatella sarasotaensis Schmelz and Portell, 2016, new species (Truncatellidae, fossil) . 15

REVIEWERS FOR VOLUME 130

Beck, Lothar

Behrens, David

Bertsch, Hans

Bieler, Riidiger

Breure, A.S.H.

Cadien, Don

Eernisse, Douglas

Fallon, Philip

Fraussen, Koen

Gerber, Jochen

Giribet, Gonzalo

Harasewych, M.G.

Herbert, David G.

Hickman, C.S,

Kiel, Steffen

Kohn, Alan

Laurent, Charles

Lee, Harry C.

1 in, Jin Xian

Mikkelsen, Paula M.

Millen, Sandra

Nekola, Jeff

Nielsen, Sven

Oleinik, Anton

Padula, Vinicius

Pearce, Timothy

Poulin, Eric

Robinson, D.G.

Rosenberg, Gary

Roth, Barry

Sigwart, Julia

Slapcinskv, John

Thiengo, Silvana

Verhecken, A.

Vermeij, Geerat |

Vilvens, C.

Watters, G. Thomas