Development, phylogeny, and taxonomy of Bostrycapulus

Zoological Journal of the Linnean Society

2005

144

75ndash101 With 11 figures

copy 2005 The Linnean Society of London


2005

144

75ndash101

75

Blackwell Science Ltd

Oxford UK

ZOJZoological Journal of the Linnean Society

0024-4082The Lin-nean Society of London 2005 2005

144

75101Original Article

SYSTEMATICS OF BOSTRYCAPULUSR COLLIN

E-mail collinrnaossiedu

Development phylogeny and taxonomy of

Bostrycapulus

(Caenogastropoda Calyptraeidae) an ancient cryptic radiation

RACHEL COLLIN

Smithsonian Tropical Research Institute Unit 0948 APO AA 34002 USA

Received February 2004 accepted for publication November 2004

Calyptraeid gastropods are well know for the taxonomic difficulties caused by their simple phenotypically variableshells In this paper I demonstrate that what was previously considered to be a single species

Crepidula aculeata

is an ancient (3ndash15 Myr) cryptic species complex made up of at least eight species and that this group should beplaced in the genus

Bostrycapulus

Despite the difficulty in finding diagnostic adult shell and anatomical featuresupon which species can be unambiguously identified DNA sequences protoconch morphology embryonic morphol-ogy and developmental characters clearly differentiate these eight species A single species with direct developmentand nurse eggs is present in the South Atlantic and a species with planktotrophic development occurs in the equa-torial Pacific The species from Japan Australia Florida the Pacific coasts of Mexico and Central America and theCape Verde Islands all have direct development Most of these species are separated by

gt

15 divergence in COIsequence data The fossil record of

Bostrycapulus

goes back to the Miocene which agrees with genetic estimates ofdivergences within the genus ranging from 3 to 15 Mya Surprisingly these ancient species differ only slightly inmorphology from each other and genetic differentiation does not correlate with geographical distance I revise thegenus

Bostrycapulus

on the basis of differences in adult morphology embryonic morphology mode of developmentprotoconch morphology and DNA sequence data I also describe four new species (

B pritzkeri

sp nov

B odites

sp nov

B latebrus

sp nov

and

B urraca

sp nov

) and remove three others (

B gravispinosus

B calyptraeformis

and

B

cf

tegulicius

) from synonymy with

B aculeatus



2005

144

75

-

101

ADDITIONAL KEYWORDS biogeography ndash

Crepidula aculeata

ndash gastropod taxonomy ndash new species ndash siblingspecies

INTRODUCTION

The application of molecular methodologies to the sys-tematics of marine invertebrates and fishes hasresulted in the discovery of numerous morphologicallycryptic species (eg Murphy 1978 Hoagland 1984Knowlton 1993 Collin 2000a Colborn

et al

2001Lessios Kessing amp Pearse 2001 Muss

et al

2001Rocha-Olivares Fleeger amp Foltz 2001 Veacuteliz Guisadoamp Winkler 2001 Wares 2001 Veacuteliz Winkler ampGuisado 2003) Cryptic species are not restrictedto plastic and morphologically simple groups likesponges and corals but occur in well-studied morpho-

logically complex groups like snapping shrimp star-fish sea urchins and fish (Knowlton 1993 Williams2000 Lessios

et al

2001 Muss

et al

2001) Geneticanalysis suggests that they may have been reproduc-tively isolated for many thousands of generations (egKnowlton amp Weigt 1998) and the occurrence of oldcryptic species shows that isolation for hundreds ofthousands to millions of years does not necessarilyresult in morphological differentiation

There are a growing number of recognized lsquoancientrsquocryptic species complexes in freshwater invertebrates(eg

Daphnia

up to 50 Myr Colbourne amp Hebert 1996Colbourne

et al

1998

Hyalella

sp complex in themid-Miocene Witt amp Hebert 2000

Brachionus plica-tilis

more than 20 Myr Goacutemez

et al

2002) althoughonly a few such radiations have been discovered in themarine environment (eg bonefish 4ndash20 Myr Colborn

76

R COLLIN



2005

144

75ndash101

et al

2001) Careful examination of morphologicallycryptic species often reveals chemical behavioural ordevelopmental differences further supporting theirstatus as distinct species (Knowlton 1993) Such dif-ferences demonstrate that there has been adequatetime for divergence to occur despite the observed mor-phological stasis

Calyptraeid gastropods are one such group wheremorphological characters cannot always be used todiscriminate effectively among species The simplicityand plasticity of calyptraeid shells has led to muchtaxonomic uncertainty and instability in this family(Hoagland 1977 1984 1986 Collin 2000a 2002Veacuteliz

et al

2001 2003) Anatomical features can beused to distinguish among major species groupswithin some genera but are very conservative andoften cannot be used to distinguish between closelyrelated species (Collin 2003a) Genetic and develop-mental features appear to diverge more rapidly thando morphological characters Therefore it is not sur-prising that recent work with the genetics and devel-opment of

Crepidula

and

Crucibulum

has led to therecognition and formal description of several morpho-logically cryptic species (eg Gallardo 1979 Hoag-land 1984 Collin 2000a 2002 Veacuteliz

et al

2001)High-level phylogenetic analyses of calyptraeids

have led to the discovery of a group of eight crypticspecies all of which were most recently ascribed to

Crepidula aculeata

(Gmelin 1791) (Hoagland 1977)

Crepidula aculeata sl

has a distinctive shell shape itis one of the few lsquo

Crepidularsquo

that retains clear tracesof coiling the shelf has a distinctive longitudinalridge and the shell often has numerous spines (Fig 1)The shells are distinct enough to have been attributedto a separate subgenus

Bostrycapulus

Olsson amp Har-bison 1953 which has sometimes been raised togenus level Phylogenetic analyses of calyptraeidsbased on anatomical (70 species Collin 2003a) andmolecular (94 species Collin 2003b) data show thatspecies in the

aculeata

group fall outside

Crepidulas

s

and are more closely related to

Crucibulum

and

Crepipatella

Therefore they should be referred to

Bostrycapulus

In her review of

Crepidula

Hoagland (1977) synon-ymized all the named species with shell characteris-tics that place them in the lsquoaculeatarsquo group with

C aculeata

but noted that it was unusual for a singlespecies without planktonic larvae to have such a widedisjunct geographical distribution After more exten-sive work with development she removed samplesfrom Panama which she called

C echinus

(Broderip1834) from synonymy with

C aculeata

withoutexplaining the change in nomenclature (Hoagland1986) My previous phylogenetic analyses ofcalpytraeids have included individuals of what appearto be several species in this group (labelled as lsquocf

aculeatarsquo in Collin 2003a b) Here I present morpho-logical developmental genetic and biogeographicaldata with the following aims (1) augmenting thedescription of

Bostrycapulus

(2) determining the rela-tionships between the different species within

Bostry-capulus

and (3) clearly delimiting the species withinthe genus

MATERIAL AND METHODS

Locality information for the live-collected specimensthat were examined or sequenced for this study arelisted in Table 1 Vouchers are deposited at the FieldMuseum of Natural History Chicago USA The Nat-ural History Museum London England and theAcademy of Natural Sciences Philadelphia USA Pro-toconchs were obtained from the same populationsexcept for the Japanese animals which were obtainedfrom shells provided by K Noda from MinabeWakayama Prefecture and Cape Verdian animalswhere protoconchs were obtained from shells providedby Emilio Rolaacuten from Rife de Chaves Sal Rei Bay BoaVista Numerous museum lots of mostly dry materialwere examined from FMNH ANSP CAS NMPNMNZ USNM AMS BMNH and IZUA Museumabbreviations follow Leviton

et al

(1985)A 611 base pair fragment of the mitochondrial cyto-

chrome oxidase I (COI) gene and a fragment of mito-chondrial 16S rDNA were sequenced for individualsfrom each locality and deposited in GenBank As thesedata were originally obtained for interspecific phylo-genetic analysis few individuals were sequenced foreach locality and in several cases only a single etha-nol-preserved individual was available for sequencing(eg

B

cf

tegulicius

) DNA was extracted from etha-nol-preserved tissue with Puregene (Gentra Systems)or DNeasy (Quiagen) extraction kits amplified usingReady-To-Go PCR beads (Pharmacia Biotech) andprimers and PCR profile of Folmer

et al

(1994) and16sar

-

16sbr of Palumbi (1996) PCR products weresequenced in both directions with dRhodamine (Per-kin Elmer) or Big Dyes cycle sequencing dye termina-tor kits using the amplification primers and an ABI377 automated sequencer Sequences were alignedusing Sequencher 30 and alignments were adjustedby eye

Phylogenetic analyses were conducted usingPAUP v 4b02 (Swofford 1998) An equal-weightedunrooted parsimony analysis was performed withgaps coded as a fifth character using a heuristicsearch with TBR branch swapping and 1000 randomadditions Bootstrap support for each clade wasassessed based on 1000 bootstrap replicates withTBR branch swapping and ten random additions Iincluded

Crepipatella lingulata

C capensis

and

Cru-cibulum auriculum

three close outgroups of

Bostry-

SYSTEMATICS OF

BOSTRYCAPULUS

77



2005

144

75ndash101

Figure 1

Photographs of (A)

Bostrycapulus calyptraeformis

from Venado Beach in Panama and (B)

B odites

sp nov

from the subtidal of Playa Orengo (the three shells on the right) and the intertidal zone of nearby San Antonio Oeste (theshell on the left) Argentina Both plates show the variation in shell colour and spine development found in samples col-lected from the same site Samples from within a site do not differ in more than three or four base pairs in COI sequencesScale bars

=

10 mm

A

B

78

R COLLIN



2005

144

75ndash101

Tab

le 1

Su

mm

ary

of li

ve-c

olle

cted

mat

eria

l use

d fo

r ob

serv

atio

ns

of d

evel

opm

ent

and

anat

omy

and

for

DN

A s

equ

enci

ng

Abb

revi

atio

ns

BM

SM

Bai

ley-

Mat

thew

sS

hel

l M

use

um

K

LK

C K

L K

aise

r C

olle

ctio

n

Spe

cies

Loc

alit

yM

ode

of d

evel

opm

ent

Vou

cher

nos

G

enba

nk

nos

CO

IG

enba

nk

nos

16S

B a

cule

atu

s

M

ote

Mar

ine

Lab

orat

ory

Lid

o K

ey

Flo

rida

U

SA

27

infin

20

cent

N

82

infin

42

cent

W[

gt

30 a

nim

als]

Dir

ect

(obs

erve

d)A

NS

P A

1974

5F

MN

H 2

8236

5B

M20

0104

55

AY

0617

92 A

Y61

8322

-3A

Y06

1774

Har

bor

Bra

nch

Oce

anog

raph

icIn

stit

ute

F

lori

daU

SA

28

infin

29

cent

N 8

1

infin

20

cent

W [

3 an

imal

s]

Dir

ect

(obs

erve

d)F

MN

H 3

0648

1A

Y61

8317

ndash

Flo

rida

Key

s U

SA

24

infin

40

cent

50

cent

N

82

infin

16

cent

02

cent

W [

2 an

imal

s]D

irec

t (o

bser

ved)

FM

NH

282

284

AY

0617

77ndash

Aba

co B

aham

as 2

6

infin

42

cent

56

cent

N

77

infin

14

cent

33

cent

W [

5 an

imal

s]N

ot o

bser

ved

BM

SM

262

92B

MS

M 2

6293

B

MS

M 2

6294

BM

SM

262

95

AY

6183

46-7

ndash

B g

ravi

spin

osu

s

Ch

ijiw

a N

agas

aki

Japa

n[1

an

imal

]N

ot o

bser

ved

FM

NH

282

336

AY

0617

83A

Y06

1766

B c

alyp

trae

form

is

Pla

ya V

enad

o P

anam

a 8

infin

55

cent

N

79

infin

38

centW [

gt10

0 an

imal

s]P

lan

ktot

roph

ic(o

bser

ved)

FM

NH

282

273

AN

SP

A19

740

BM

2001

0452

AY

0617

86 A

Y61

8328

AY

6183

34-4

0

AY

6183

42-5

AY

0617

77 A

Y61

6674

Isla

Ray

a A

zuer

o P

enin

sula

P

anam

a 7

infin23

64centN

80infin

160

2centW

Dir

ect

(obs

erve

d)F

MN

H 3

0648

2A

Y61

8327

AY

6166

73

Kan

eoh

e B

ay H

awai

i U

SA

[5 a

nim

als]

Pla

nkt

otro

phic

(B

ell

1993

)F

MN

H 2

8217

1-2

AY

0617

90A

Y06

1769

US

S M

ach

inis

t G

uam

[3

anim

als]

Not

obs

erve

dF

MN

H 2

8236

2A

Y06

1791

AY

0617

71Z

orri

tos

Per

u

3infin45

centS

80infin4

0centW

[20

anim

als]

Pla

nkt

otro

phic

(obs

erve

d)F

MN

H 2

8236

7A

Y06

1778

AY

0617

73

Los

Au

baz

Pai

ta P

eru

5infin1

0centS

81infin1

0centW

[20

an

imal

s]P

lan

ktot

roph

ic(o

bser

ved)

AN

SP

A19

746

FM

NH

28

2351

BM

2001

0454

AY

0617

85

AY

6183

29-3

2A

Y06

1772

B c

f te

guli

ciu

sC

alh

eta

Fu

nda

S

al I

slan

d C

ape

Ver

de

16infin4

0centN

22

infin03cent

W[1

an

imal

]

Dir

ect

(fro

mpr

otoc

onch

)F

MN

H 2

8235

9A

Y06

1776

AY

0617

75

SYSTEMATICS OF BOSTRYCAPULUS 79

copy 2005 The Linnean Society of London Zoological Journal of the Linnean Society 2005 144 75ndash101

B p

ritz

ker

i E

dwar

ds B

each

Syd

ney

Au

stra

lia

33

infin51cent

S 1

51infin1

3centE

[14

an

imal

s]T

YP

E L

OC

AL

ITY

Dir

ect

(obs

erve

d)F

MN

H 2

8230

2 A

NM

C40

0000

AY

0617

93 A

Y61

8348

AY

0617

67

B o

dit

es

Pla

ya O

ren

go n

ear

San

An

ton

ioO

este

Arg

enti

na

40infin

53centS

64

infin29cent

W [

gt25

an

imal

s]

Dir

ect

wit

h n

urs

eeg

gs (

obse

rved

)F

MN

H 2

8229

7A

NS

P A

1974

4B

M20

0104

56

AY

0617

82 A

Y06

1784

A

Y06

1794

AY

0617

62 A

Y06

1764

Woo

leyrsquo

s P

ool

Mu

izen

berg

Sou

thA

fric

a 3

4infin04

centS

18infin2

0centE

[15

anim

als]

TY

PE

LO

CA

LIT

Y

Dir

ect

wit

h n

urs

e eg

gs(o

bser

ved)

FM

NH

282

277

V94

47

T17

83 B

M20

0104

53A

Y06

1780

AY

0617

88ndash

Por

t E

liza

beth

Sou

th A

fric

a[2

an

imal

s]N

ot o

bser

ved

FM

NH

282

368

AY

0617

87A

Y06

1765

Goi

s B

each

San

tos

Bay

Satildeo

Pau

lo

Bra

zil

24infin

00centS

46infin

21centW

[5 a

nim

als]

Dir

ect

wit

h n

urs

eeg

gs (

from

prot

ocon

ch)

FM

NH

282

350

AY

0617

79 A

Y06

1781

AY

0617

63

B l

ate

bru

sE

l C

omit

aacuten n

ear

La

Paz

BC

SM

exic

o 2

4infin07

centN

110infin

24centW

[10

anim

als]

TY

PE

LO

CA

LIT

Y

Dir

ect

(obs

erve

d)F

MN

H 2

8219

3-4

AY

0617

89 A

Y61

8333

AY

0617

68

B u

rra

ca

Isla

Par

ida

Gu

lf o

f C

hir

iqu

iP

anam

a 8

infin54

58centN

82

infin18

671cent

W[

gt50

anim

als]

TY

PE

LO

CA

LIT

Y

Dir

ect

(obs

erve

d)A

NS

P 4

1217

8ndash9

FM

NH

306

483

AY

6183

19 A

Y61

8325

-6A

Y61

6667

-9

Isla

Ray

a A

zuer

o P

enin

sula

P

anam

a 7

infin23

64centN

80infin

160

2centW

Dir

ect

(obs

erve

d)F

MN

H 3

0648

4A

Y61

8321

ndash

Isla

Jac

aron

Par

que

Nat

ion

alC

oiba

P

anam

a 7

infin19

10centN

81

infin43

83centW

[3

anim

als]

Not

obs

erve

dK

LK

C I

CP

-03ndash

069

AY

6183

18 A

Y61

8320

A

Y61

8324

ndash

El

Sal

vado

r G

ulf

of

Fon

seca

13

infin26

4 N

89infin

480

4 W

[3 a

nim

als]

13infin1

723

N 8

9infin18

07

W [

1 an

imal

]N

ot o

bser

ved

AN

SP

412

180-

1A

Y61

8341

AY

6183

49A

Y61

6670

-2

Spe

cies

Loc

alit

yM

ode

of d

evel

opm

ent

Vou

cher

nos

G

enba

nk

nos

CO

IG

enba

nk

nos

16S

80 R COLLIN


capulus (see Collin 2003b) and used them to root theanalysis Genetic distances were calculated usingKimura 2-parameter distances

DNA sequence data were also analysed using aBayesian approach The appropriate model and start-ing parameters for Bayesian analysis were chosen foreach of the datasets using the likelihood ratio testimplemented in ModelTest 306 (Posada amp Crandell1998 2001) with the default settings and an a-levelof 001 Bayesian analyses using MrBayes 201(Huelsenbeck 2000 Huelsenbeck amp Ronquist 2001)were conducted for each dataset (COI 16S and COIand 16S combined) using the model obtained fromModelTest 306 The Bayesian analysis using one coldand three incrementally heated chains started from arandom tree with a uniform prior for branch lengthsand for the Gamma shape parameter Invariant siteswere retained in the sequences and their frequencywas estimated using the lsquoinvgammarsquo setting TheMetropolis-coupled Markov chain Monte Carlo (MCM-CMC) analysis was run five times for 1000 000 gener-ations for each dataset and the number of trees to bediscarded as representing a lsquoburn-inrsquo period was deter-mined graphically to be either 25 000 or 50 000 gen-erations Majority-rule consensus trees for every 50thtree after the lsquoburn-inrsquo period were created usingPAUP and consensus phylograms were created inMrBayes

The morphology and anatomy of ethanol- or forma-lin-preserved individuals were examined under a WildM4 dissecting microscope The anatomy of five to tenanimals was examined from most localities Prior tomounting for scanning electron microscopy proto-conchs and radulae were cleaned briefly in dilutebleach and rinsed in distilled water All specimenswere gold-coated and viewed with an Almary scanningelectron microscope Two to five radulae from eachlocality were prepared for SEM To estimate within-individual variation the number of denticles on eachtooth were counted for ten rows of unworn teeth perindividual

Developmental stages were observed live and mea-sured with dissecting and compound microscopesBroods from more than 30 animals were observedfrom Argentina and Panama and five to ten broodswere observed for populations from Florida PeruSouth Africa Sydney and Mexico Developmentalstages were not available for animals from JapanBrazil or Cape Verde Larvae of the single specieswith planktonic development were raised according tothe methods of Collin (2000b)

RESULTS

The animals examined during this study can be attrib-uted to eight species on the basis of protoconch mor-

phology developmental biology embryology and DNAsequence data

DNA SEQUENCE DATA

Phylogenetic analysis of COI and 16S DNA sequencedata shows little sequence variation within each local-ity (about 05ndash1 in COI) There are eight distinctclades (species) that differ from each other by 6ndash21in COI sequences and by at least 2 in 16S sequences(Fig 3 Table 2) These groups are supported as mono-phyletic with bootstrap and Bayesian support above98 and 100 respectively (Fig 2) Sequence diver-gences of such magnitude commonly occur betweenmorphologically well-differentiated species of calyp-traeids (Collin 2003a b)

Four of these clades include samples for severallocations One clade is composed of sequences fromindividuals collected from the South Atlantic (BrazilArgentina and South Africa) it shows 08ndash12 COIdivergence between localities Another clade includessamples from the Bay of Panama Hawaii and Guamwhich are identical to each other and also includes theclosely related (4 divergent) material from Peru(Figs 2 4 Table 2) The third contains samples fromboth coasts of Florida and the Bahamas The fourthincludes material from the Pacific coast of El Salvadorand the western half of Panama Animals from thisclade occur in sympatry with the Panama-Hawaiiclade in the Perlas Archipelago and the Azuero Penin-sula Panama Samples from the remaining localitiesform their own individual clades

Analyses of the individual gene sequences and thecombined analysis show Bostrycapulus to be mono-phyletic (as did two much larger analyses Collin2003a b) However the relationships between the dis-tinct clades within the genus are not well resolved Inall analyses there is high support for the result thatthe Florida-Bahamas clade is sister to the samplefrom Cape Verde and that these two are sister toremaining taxa The samples from Baja CaliforniaSydney and Japan group together with 100 boot-strap and Bayesian support but the relationshipsbetween them are unresolved The relationship of thisPacific clade with the two Panamanian species and theSouth Atlantic species is unresolved

MORPHOLOGY

Shell morphology and colour are variable within eachpopulation Some sympatric individuals have numer-ous fine spines some have fewer large spines Someshells are robust some are small and gracile (Fig 1)Shells collected subtidally from Playa Orengo Argen-tina are usually completely smooth although somehave numerous large robust spines Shells from the



Figure 2 The Bayesian best estimate topology of the phylogeny of Bostrycapulus based on COI Numbers above thebranches represent bootstrap percentages and those below the branches are Bayesian support Branches are labelled withthe collecting locality and the individual code = type individual

genetically similar animals from Brazil do not sharethis feature and animals with identical COIsequences collected from the intertidal zone of nearbySan Antonio Oeste are smooth and almost black(Fig 1) Shell colour is also variable Shells are oftendark brown with a wide pale streak running slightlyto the right of the midline although all populations

also contain animals with uniformly pale shells(Fig 1) Animals with pale shells also have pale bod-ies In all populations the shelf is usually white butsometimes has brown streaks All of the ethanol-preserved material available to me from South AfricaMexico and Japan is so over-grown with corallinealgae and other fouling organisms that the details of

82 R COLLIN


Tab

le 2

P

airw

ise

Kim

ura

2-p

aram

eter

gen

etic

dis

tan

ces

betw

een

in

divi

dual

s fr

om e

ach

loc

alit

y B

old

valu

es i

ndi

cate

in

tras

peci

fic

com

pari

son

s A

bbre

viat

ion

sA

rg A

rgen

tin

a B

ah B

aham

as

BP

Bay

of

Pan

ama

CT

Cap

e T

own

CV

Cap

e V

erde

E

S E

l S

alva

dor

GC

Gu

lf o

f C

hir

iqu

i

16S

CO

IC

VB

razi

lC

TA

rgJa

pan

Per

uB

PH

awai

iG

uam

Mex

ico

Flo

rida

Syd

ney

Bah

ES

GC

CV

ndash0

081

007

80

083

007

60

080

008

10

081

008

00

074

003

40

074

ndash0

068

007

5B

razi

l0

168

ndash0

062

000

60

067

005

10

054

005

40

054

006

90

073

007

0ndash

004

10

045

CT

016

60

012

ndash0

008

006

50

045

004

70

047

004

70

067

007

10

067

ndash0

038

004

3A

rg0

174

000

80

010

ndash0

069

005

40

056

005

60

056

007

20

075

007

2ndash

004

30

047

Japa

n0

211

015

80

154

015

6ndash

006

10

056

005

60

056

003

40

071

001

7ndash

005

90

068

Per

u0

185

012

60

126

012

60

174

ndash0

006

000

80

006

006

60

081

006

3ndash

005

20

054

BP

016

30

103

010

30

105

016

60

044

ndash0

002

000

00

061

008

10

059

ndash0

052

005

4H

awai

i0

166

010

30

103

010

50

166

004

60

002

ndash0

002

016

20

085

005

9ndash

005

20

056

Gu

am0

163

010

30

103

010

50

166

004

60

000

000

2ndash

016

20

085

005

9ndash

005

30

054

Mex

ico

018

60

144

014

00

138

010

60

164

016

20

061

006

1ndash

006

90

038

ndash0

073

007

7F

lori

da0

066

015

70

155

016

00

192

016

90

157

015

90

157

019

9ndash

006

9ndash

006

10

073

Syd

ney

017

40

133

012

80

131

009

40

152

014

00

140

014

00

122

017

4ndash

ndash0

056

007

2B

ah0

066

015

50

153

015

80

190

016

00

155

015

70

157

020

00

002

017

2ndash

ndashndash

ES

017

10

167

012

10

113

012

30

160

012

70

129

012

90

129

015

50

156

015

2ndash

000

8G

C0

161

011

90

111

012

10

163

012

10

123

012

30

123

016

70

152

015

60

151

000

7ndash



shell sculpture are difficult to distinguish and com-pare However examination of shells in museum col-lections suggests that such variation in shell shapecolour and spination is typical of most populations ofthese species Such variation can be found in anylarge lot from a single locality

The different species of Bostrycapulus can bedelimited on the basis of protoconch morphology Pro-toconchs do not usually remain intact on the teleo-conchs of adult animals and those that are intactoften appear worn SEMs show that juvenile shellsfrom Brazil and Argentina have large protoconchs of

Figure 3 The Bayesian best estimate topology of the phylogeny of Bostrycapulus based on 16S Numbers above thebranches represent bootstrap percentages and those below the branches are Bayesian support Branches are labelled withthe collecting locality and the individual code = type individual

Figure 4 Unrooted haplotype network of COI sequences from Bostrycapulus calyptraeformis Slashes on branches showthe number of differences between the haplotypes Branches without slashes have a length of one Size of the circles rep-resent the number of individuals with that haplotype

Peru

Panama

HawaiiGuam

84 R COLLIN


slightly more than a single whorl with irregulargrowth lines (Figs 5F 4I) typical of direct develop-ment with nurse eggs Shells from the Bay of Pan-ama and Peru have smaller more coiled protoconchstypical of planktotrophic development that increaseregularly in size (Figs 5B 4E) Protoconchs fromAustralia Cape Verde Japan the Gulf of Chiriquiand Florida (Figs 5A 4C D G H respectively) aremore globose than those from the Bay of Panamaand Peru and have less than a single whorl Asexpected from differences in egg size (see below) theprotoconchs from Australia are the most globoseGranular sculpture was evident on the protoconchsfrom Gulf of Chiriqui and Japan although no sculp-ture was evident on those obtained from juvenile or

adult shells from the other localities Shells of directdeveloping embryos that had been removed fromtheir capsules from both Australia (Fig 6) and Mex-ico showed spiral rows of fine granular sculpturewhen examined under a dissecting microscope andprehatching stages from the Gulf of Chiriqui showedwell-developed spines (Fig 7) Likewise large granu-lar sculpture is visible under a compound micro-scope on the larval shell of 1-week-old and 3-week-old larvae from the Bay of Panama (Fig 8) but thiswas not retained on the protoconchs obtained fromthe same species It is unknown for how long sculp-ture is retained after hatching or settlement How-ever its presence in early stages appears to betypical of Bostrycapulus species

Figure 5 Protoconchs A Bostrycapulus pritzkeri sp nov from Sydney B B calyptraeformis from the Perlas IslandsPanama C B cf tegulicia from Cape Verde D B gravispinosus from Minabe Wakayama Prefecture Japan EB calyptraeformis from Paita Peru F B odities sp nov from Playa Orengo Argentina G B urraca sp nov from IslaParida Panama H B aculeatus from Lido Key Florida I B odites sp nov from Satildeo Paulo Brazil All are to the samescale Scale bar = 500 mm



Figure 6 Embryos of Bostrycapulus pritzkeri sp novNote the distinctive granular shell sculpture and theabsence of a distinct velum at all stages A excapsulatedearly stage embryos at the beginning of shell formationScale bar = 150 mm B excapsulated embryos with well-developed shells showing granular shell sculpture and thesmall ridge of the velum at the base of the tentacle Scalebar = 250 mm C encapsulated embryos near hatchingwith fully developed shell and body pigmentation Scalebar = 250 mm

Figure 7 Embryos of Bostrycapulus urraca sp nov Aearly postgastrula stage where the embryo is covered witha thin ciliated epithelium B mid-veliger stage showingthe granulated shell sculpture the operculum behind thewell-developed foot the single embryonic kidneys and thereduced velum C Hatching stage showing the well-devel-oped shell sculpture Scale bar = 150 mm

86 R COLLIN


Examination of preserved samples did not show anyconsistent anatomical differences among samplesfrom the different locations The anatomy of Bostry-capulus is however distinct from the other majorcalyptraeid genera (Fig 9 Simone 2002 Collin2003a and see below) The female genital papillawhich has proven to be a useful character in distin-guishing closely related Crepidula species (Collin2000a) is absent in Bostrycapulus Radula morphology(Fig 10 Table 3) does not appear to be useful in dif-ferentiating among these groups There is significantwithin-individual variation in the number of denticleson each tooth In addition individuals collected fromthe same locality often vary in the frequency of teethwith few or many denticles as well as in the maximumand minimum number of denticles

DEVELOPMENT

Three different modes of development are observed inthe Bostrycapulus species examined here (1) plank-totrophic larvae (2) direct development with largeeggs and (3) direct development from small eggs withnurse eggs (Table 4) These differences in modes ofdevelopment and smaller differences in the details ofdevelopment correspond to the same eight clades iden-tified by the DNA sequence analysis and protoconchmorphology

The clade from the South Atlantic has direct devel-opment from small eggs which consume nurse eggsand hatch as crawling juveniles The nurse eggs beginto develop and cannot be distinguished from theembryos until after gastrulation The clade from theBay of Panama Hawaii and Peru has planktotrophicdevelopment Animals from Australia Mexico Floridaand western Panama develop directly from large eggsDirect development without nurse eggs is alsoreported for animals from Japan (Ishiki 1936) but theegg size seems too small (Ishiki 1936 Amio 1963) toproduce such large juveniles It is unlikely that these

Figure 8 A 2-week-old larva of Bostrycapulus calyptrae-formis showing the velar pigment shell sculpture (on thetop of the shell) and large foot Scale bar = 300 mmB intracapsular larva of B aculeatus showing the well-developed velum with pigment spots and body pigmenta-tion Scale bar = 200 mm

Table 3 Variability of radula characteristics of five species of Bostrycapulus

Species B aculeatus B calyptraeformis B pritzkeri B odites B latebrus

Number of animals (ten rows each) 3 2 2 5 2Number of denticles

Rachidian 2ndash3 2ndash4 2ndash4 2ndash5 2ndash3Inner side of lateral 1ndash3 1ndash3 1 1ndash3 1Outer side of lateral 5ndash8 5ndash10 6ndash12 5ndash11 4ndash7Inner side of inner marginal 2ndash7 2ndash8 6ndash10 3ndash11 2ndash5Outer side of inner marginal 0ndash6 4ndash6 4ndash8 0ndash3 1ndash4Inner side of outer marginal 0ndash3 0ndash2 3ndash8 1ndash7 0ndash4Outer side of outer marginal 0 0 0 0 0



Figure 9 Illustrations of anatomy of Bostrycapulus drawn from observations of several animals of B odites sp novfrom Argentina There are no differences among species in the characters depicted here A dorsal view of the animal sub-sequent to removal from the shell B dorsal view of the animal with the mantle reflected C osphradium D penis Abbre-viations cg capsule gland ct ctenidia dg digestive gland e oesophagus f foot fp food pouch g seminal groovegd gonad hg hypobranchial gland i intestine k kidney nr nerve ring os osphradium sg salivary gland sm shell mus-cle ss style sac st stomach v ventricle

A B

C D

DISCUSSION

Although the populations examined here cannot beeasily distinguished on the basis of shell morphologyor easily visible anatomical features the availabledata show that at least eight distinctly different mito-chondrial haplotype lineages are present in Bostry-capulus The levels of intraspecific DNA sequencedivergence reported for other calyptraeid species(Collin 2000a 2001) are similar to the divergencesbetween sequences reported here for individualsbelonging to the South Atlantic clade or to the equa-torial Pacific clade Genetic divergences between eachof the eight clades are considerably greater thandivergences between cryptic sibling species of othercalyptraeids (Collin 2000a 2001) and they are infact often much larger than divergences betweenmany clearly defined species of Crepidula (Collin2003a b) The only other anatomical work that exam-ined and compared several of these clades (animalsfrom Spain Brazil Hawaii and Sydney Simone2002) also found no consistent morphological differ-ences among populations Such cryptic differentiation

Figure 10 Radula of Bostrycapulus aculeatus collectedfrom Mote Florida Scale bar = 100 mm

differences in development are the result of interspe-cific variation as poecilogony is not known in caeno-gastropods (Hoagland amp Robertson 1988 Bouchet1989) and no variation in development was observedamong individuals from a single locality More detailsof embryology are given below with the descriptions ofeach species

88 R COLLIN


Tab

le 4

S

um

mar

y of

Bos

tryc

apu

lus

spec

ies

Dia

gnos

tic

feat

ure

s ar

e h

igh

ligh

ted

in b

old

text

A

bbre

viat

ion

s s

s s

pira

l sc

ulp

ture

B a

cule

atu

sB

gra

visp

inos

us

B c

alyp

trae

form

isB

teg

uli

ciu

sB

pri

tzke

riB

od

ites

B l

ateb

rus

B u

rrac

a

Au

thor

ity

(Gm

elin

179

1)(K

uro

da amp

Hab

e 1

950)

(Des

hay

es 1

830)

(Roc

heb

run

e18

83)

sp n

ov

sp n

ov

sp n

ov

sp n

ov

Fate

of

type

St

Pet

ersb

erg

un

know

nP

aris

Mu

seu

mP

aris

Mu

seu

mA

ust

rali

anM

use

um

Nat

alM

use

um

Fie

ld M

use

um

Fie

ld M

use

um

Typ

e lo

cali

tyM

iddl

eA

mer

ican

Isla

nds

Hir

ado

Is

Nag

asak

iP

ref

Japa

n

Per

u (

dubi

ous)

Sen

egal

Edw

ards

Ree

fS

ydn

ey

Au

stra

lia

Woo

leyrsquo

s P

ool

Cap

e T

own

S

A

La

Paz

BC

SM

exic

oG

ulf

of

Ch

iriq

ui

Pan

ama

Dev

elop

men

tdi

rect

dire

ctp

lan

kto

trop

hic

dire

ct (

from

prot

ocon

ch)

dire

ctd

irec

t w

ith

nu

rse

eggs

dire

ctdi

rect

Egg

siz

e (m

m)

380

(Hoa

glan

d 1

986)

200

(qu

esti

onab

le)

180

ndash53

0ndash56

019

848

837

0

(Am

io 1

963)

Hat

chin

g si

ze(m

m)

840

1000

ndash120

0 38

0ndash

ndashndash

ndash88

8(H

oagl

and

198

6)(I

shik

i 19

36)

Em

bryo

nic

oper

culu

mpr

esen

tndash

pres

ent

ndashab

sen

tpr

esen

tpr

esen

tpr

esen

t

Dis

tin

ct v

elu

mw

ith

foo

dgr

oove

med

ium

spo

tted

w

ith

foo

d gr

oove

ndashla

rge

pig

men

ted

ndashab

sen

tsm

all

un

pigm

ente

dsm

all

un

pigm

ente

dab

sen

t

Em

bryo

nic

sh

ell

scu

lptu

regr

anu

lar

ss

ss a

t h

atch

ing

(Am

io)

fin

e sp

ines

ove

ren

tire

lar

val

shel

l

ndashgr

anu

lar

sssm

ooth

wit

hir

regu

lar

grow

thli

nes

gran

ula

r ss

gran

ula

r ss

Pro

toco

nch

1 w

hor

l1

wh

orl

15

wh

orls

less

th

an 1

w

hor

ln

ot a

vail

able

125

wh

orls

less

th

an 1

w

hor

lle

ss t

han

1w

hor

lL

ocal

itie

sF

lori

da Y

uca

tan

B

aham

asJa

pan

Per

u

Pan

ama

Haw

aii

Gu

amW

est

Afr

ica

Cap

e V

erde

Is

Au

stra

lia

Sou

th A

fric

a

Pat

agon

ia

Bra

zil

La

Paz

Mex

ico

Pan

ama

El

Sal

vado

r



is not unusual or unexpected among calyptraeid spe-cies (eg Gallardo 1979 Collin 2000a 2001 Veacutelizet al 2001 2003) but the large number of crypticspecies is unusual

The results presented here suggest that Bostrycapu-lus shows as much among-species genetic divergencein the Pacific as in the Atlantic (eg 162 COI diver-gence between Panama and Mexico and 168between Cape Verde and Brazil Table 2) The maxi-mum levels of genetic divergence (21) between Bos-trycapulus species are similar to or somewhat greaterthan those reported for other widespread marine gen-era 4ndash6 in cytochrome b from trumpet fish species(Bowen et al 2001) 2ndash19 in ATPase and COI fromDiadema species (Lessios et al 2001) 8ndash20 in COIfrom Eucidaris (Lessios et al 1999) up to 16 incytochrome b from Ophioblennius fish (Muss et al2001) up to 23 in COI from Chthamalus barnacles(Wares 2001) In most of these cases however thespecies can be distinguished on morphological groundsand have been historically recognized as distinct Thehigher levels of genetic divergence and almost com-plete absence of morphological differentiation amongBostrycapulus species suggest that the rate of morpho-logical evolution relative to genetic change is consid-erably slower in calyptraeids than it is in these othergroups

There is ample evidence that the radiation of Bos-trycapulus is an ancient cryptic radiation like thatdocumented for bonefish (Colborn et al 2001)Museum records place Bostrycapulus as far back asthe Miocene in Florida and California (Hoagland1977) Application of two separately derived molecularclock rate estimates to the divergences listed inTable 2 provides similar rough estimates of the age ofthe group and also places it well into the MioceneApplication of a rate calibration of 088Myr for COIof cowries (C P Meyer unpubl data) gives the diver-gence times among the eight Bostrycapulus lineagesas 37ndash120 Myr Application of Markorsquos (2004) rate of22 substitutions per base per year for mitochondrialthird positions in Nucella dates the divergences at37ndash15 Myr Because the fossil record of Bostrycapulusis poor and because none of the sister-species pairs dis-covered here are separated by well-dated barriers likethe Isthmus of Panama it was not possible to calibratethe Bostrycapulus sequences

The geographical range of marine invertebrates isusually assumed to be related to mode of developmentSpecies with direct development are presumed to havehigher levels of population structure and smallergeographical ranges than those with planktotrophicdevelopment These expectations do not appear to beborne out in the case of Bostrycapulus The directdeveloping species in the South Atlantic show very lit-tle genetic differentiation over a large geographical

range COI sequences show less differentiationbetween these South African and South American pop-ulations than is present over hundreds of kilometresalong the east coast of North America in other directdeveloping Crepidula species (Collin 2001) It isunlikely that the genetic similarity of populations inArgentina Brazil and South Africa is due to recentunrecorded introductions Fossil lsquoC aculeatarsquo havebeen collected from the Pliocene and Pleistocene ofArgentina (Hoagland 1977) and the Pleistocene ofSouth Africa (R Kilburn pers comm) The placementof the South African populations as sister to the othertwo suggests that the trans-Atlantic dispersal eventpredates the COI coalescence of the Argentine andBrazilian populations It is possible that animals couldbe transported between South America and SouthAfrica on the holdfasts of drifting Ecklonia spp Dur-villaea antarctica and Marcrocystis pyrifera kelp(Smith 2002) Individuals of a Bostrycapulus specieshave been found attached to holdfasts of such kelp (RKilburn pers comm) as have the brooding bivalveGaimardia trapesina (Lamarck 1819) (Helmuth Veitamp Holberton 1994) Widely dispersed marine speciesare not uncommon in the southern hemisphere (egWaters amp Roy 2004)

The clade in the equatorial Pacific shows genetic dif-ferentiation between Peru and Panama but not overthe thousands of kilometres between Hawaii Guamand Panama (Figs 2 4) The Bayesian estimate of COIphylogeny (Fig 2) shows the clade from Peru nestedwithin the Panama haplotypes while the estimatebased on 16S shows the clades as sisters suggestingthat the root of the Peru clade has been misplaced inthe phylogeny The unrooted haplotype network(Fig 4) shows that the two clades are reciprocallymonophyletic and that the Hawaiian and Guam hap-lotypes nest firmly within the Panamanian clade

It is probable that the genetic similarity betweenthe geographically distant populations in GuamHawaii and Panama is the result of human-mediatedintroductions For example the samples from Guamthat were used in this study were obtained from a drydock after its arrival from Hawaii Because Bostry-capulus has not historically been present in Guam (GPaulay pers comm) these animals may represent thefounders of a new biological invasion LikewiseB aculeatus is often listed as an introduced speciesin Hawaii (Coles et al 2000) and the earliest recentmaterial appears to have been collected in Hawaii in1915 However Sowerby (1883) and Reeve (1859) bothlist lsquoCrepidula aculeatarsquo as occurring in the lsquoSandwichIslandsrsquo (presumably the Hawaiian Islands and notSouth Sandwich) Pleistocene material that is possiblyattributable to Bostrycapulus from Hawaii is depos-ited at ANSP (ANSP 116536) but is in such poor con-dition that it is not possible to identify it with

90 R COLLIN


certainty Animals identified as B aculeatus have alsobeen collected in Alicante Spain (Simone 2002) anarea outside their historical range Unfortunately thephylogenetic affinity of these animals within Bostry-capulus is unclear and diagnostic material is not cur-rently available for study The possible and realizedpotential for Bostrycapulus species to become estab-lished invaders makes the documentation of naturalranges and clarification of species identifications ofpressing concern

TAXONOMIC DESCRIPTIONS

I feel that it is necessary to formally recognize each ofthe clades recovered in this study as distinct speciesdespite the difficulty in finding diagnostic features inadult morphology There is no theoretical reason toexpect that mechanisms of speciation should alwaysresult in species that can be distinguished visually Ibelieve that the high levels of genetic differentiationamong the samples examined here the clear differ-ences in development and the large geographical sep-arations strongly support the status of these differentclades as separate species Continued applicationof the B aculeatus sl concept would only furtherobscure data that could possibly be used to distinguishthese species as they come to light as well as limitingour ability to identify species introductions and extinc-tions (eg Geller et al 1997 Geller 1999) Applicationof the available names for the species from Japan theequatorial Pacific and West Africa without formallynaming the other clades would leave a poly- and para-phyletic B aculeatus a clearly undesirable situationTherefore I remove the available names from synon-ymy with B aculeatus and formally describe four newspecies I take a conservative approach and describenew species only if a putative species differs fromother groups in development and forms a topologicallywell-defined monophyletic clade in the mitochondrialgene trees This approach discounts the possibilitythat the low levels of genetic differentiation within theSouth Atlantic and the equatorial Pacific clades reflectadditional poorly differentiated species Further studyand greater geographical sampling is necessary todetermine the status of these populations

Hoagland (1977) synonymized a number ofspecies with B aculeatus (Gmelin 1791) HoweverC tomentosa C maculata and C foliacea need to beremoved from this synonymy and should not be placedin Bostrycapulus Examination of the original descrip-tions and type material shows that C tomentosa Quoyamp Gaimard 1832-33 (see Hoagland 1983) andC maculata Quoy amp Gaimard 1832-33 are both moresimilar to Calyptraea or Sigapatella than they are toBostrycapulus They have a cap-shaped shell with acentral apex and obvious coiling The thick shaggy

periostracum gives the impression that the shells arespiny The figure with the original description and thetype material of C foliacea (Broderip 1834) are moresimilar to Crepipatella fecunda or Crepipatelladilatata and are also clearly not allied with Bostry-capulus Broderip (1834) placed this species in Crepi-patella which appears to be a more appropriatedesignation

The following eight species are recognized hereas members of Bostrycapulus B aculeatus (Gmelin1791) B gravispinosus (Kuroda amp Habe 1950)B calyptraeformis (Deshayes 1830) B cf teguliciusB pritzkeri sp nov B odites sp nov B latebrus spnov and B urraca sp nov

Crepidula holiotoidea Fischer von Waldheim 1807(non Crepidula haliotoidea Marwick 1926) is alsoclearly a Bostrycapulus species (not a synonym ofC dilatata (Ivanov et al 1993)) but I consider it anomen dubium because the type locality is unknown(Ivanov et al 1993) and the lack of diagnostic shellcharacters in any of the species in this complex makeit impossible to assign material other than the lecto-type to C holiotoidea with any confidence The nameC californica Tryon 1886 also refers to an animal inthis group but it is a nomen nudum Neither of thesenames will be considered further

According to museum records shells fitting thedescription of Bostrycapulus species have been col-lected from the Galapagos Islands the MarquesasVenezuela Cuba Chile Senegal India and Koreaalthough no observations of development or moleculardata are available for samples from these placesDespite recent concerted efforts no live animals havebeen collected from Chile (pers observ D Veacuteliz amp OChaparro pers comm) or southern Peru (persobserv A Indacochea pers comm) despite materialat the ANSP listing a locality of lsquoCallao Perursquo There-fore the occurrence of these animals in Chile andsouthern Peru may be episodic Clearly further sam-pling of these taxa including developmental andmolecular characters would contribute significantlyto our understanding of their evolution biogeographyand taxonomy

BOSTRYCAPULUS OLSSON amp HARBISON 1953

Type species Bostrycapulus aculeatus (Gmelin) byoriginal designation

Original descriptionlsquoShell widely slipper-shaped with a strongly eccentricapex closely appressed and spirally coiled towards theleft side (viewed dorsally) Surface with strong radialriblets or threads the primary ones often becomingscabrous or spiniform Diaphragm as in Crepidula ss



its edge nearly straight the muscle scar below smallbut distinctrsquo

Morphological descriptionShell externally the shell is relatively flattened andmore coiled but generally similar to that of Crepidulaspecies The internal septum extends about half thelength of the shell and the anterior margin isindented medially and notched on the animalrsquos leftside A distinct but small medial ridge or creaseextends from the medial indentation to the posteriorshell margin near the apex The small lunar musclescar on the animalrsquos right side anterior to the shelf isoften more deeply indented than in Crepidula speciesThe shell is distinctly coiled with about one singlewhorl after the protoconchndashteleoconch boundary Theapex is appressed usually occurring slightly above theposterior shell margin on the right it is not excavatedExternal shell sculpture ranges from widely spacedlarge scale-like plicate spines to tightly packedpointed granular bumps along fine spiral ribs Shellcolour ranges from overall cream with scattered brownmarkings to solid chocolate brown sometimes with apale streak and occasionally solid tan The markingsare sometimes speckled and often streaky No teleo-conch characters have been found to unambiguouslydiagnose species in the genus

Protoconch the size of the protoconch varies betweenspecies depending on the mode of development but isless than two whorls and is often eroded in adult spec-imens Hatchlings and embryos show a linear patternof fine widely spaced granules on the protoconch Pro-toconch characters can be used to diagnose severalspecies

Pigmentation the head neck foot and mantle arecream but there is a matt black marbled area alongthe edge of the foot Large yellow or orange splotchesare scattered along the neck lappets and concentratedon the lips and tentacles Black pigment also occurs onthe dorsal side of the head and neck The intensity ofall pigmentation varies with some animals showingalmost no black pigment The black pigment isretained in preserved or fixed material although theyellow and orange markings are lost There are nodiagnostic differences in pigmentation among the spe-cies described here

Anatomy the overall anatomy of Bostrycapulus sppis similar to that of other calyptraeids (Kleinsteuber1913 Werner amp Grell 1950 B aculeatus sl describedby Simone (2002) (Fig 9)) The foot is round with arectangular propodium and extends slightly morethan half the length of the shell There are no meso-podial flaps The corners of the propodium are not

extended laterally and cannot extend free of the rest ofthe foot The neck is dorsoventrally flattened with lap-pets along each side and with a narrow food groovetravelling forward to the tentacle on the right sideTentacles are stubby with a simple black eye on thelateral side about a third of the way to the distal endThe lips are equal in size with small thin jaws embed-ded in the dorsal side Tentacles narrow suddenlyimmediately distal to the eye The food pouch at theanterior medial edge of the mantle is surrounded bythick flaps The tissue connection between the mantlemargin and the foot extends anterior to the foot and tothe shelf on the animalrsquos left side The osphradium isa dark tightly packed strip of bipectinate filaments atthe base of the gill filaments The anterior filamentsare smaller than the posterior filaments The osphra-dium extends from the food pouch to slightly withinthe mantle cavity The long narrow gill filaments aresomewhat thickened at their base The salivary glandsare huge filling the entire neck and extending fromthe buccal mass externally past the nerve ring to theanterior margin of the visceral mass They are intri-cately branched along their entire length

When removed from the shell the distal third of theviscera curves to the animalrsquos right The tapered man-tle cavity and gills extend about two thirds of the wayto the tip of the viscera on the dorsal left side Thecrescent-shaped shell muscle extends dorsally fromthe foot to the shell roof on the right side A small dor-sal attachment muscle runs from within the dorsalmantle tissue above the intestine to the medial shellroof just anterior to the shelf

The stomach is visible dorsally to the right of theposterior end of the mantle cavity The oesophagusruns ventrally in the viscera and enters the stomachposteroventrally The short style sac runs laterallyfrom the stomach to the left margin of the visceralmass in the dorsal viscera posterior to the mantle cav-ity The distal end of the style sac narrows to connectwith the intestine which runs directly to the right sidein the ventral visceral mass The distal loop of theintestine is visible in the dorsal wall of the mantle cav-ity This arrangement of the digestive system withrespect to the mantle cavity is distinct from thearrangement in Crepidula where the mantle cavityextends to the end of the visceral mass and the stylesac is ventral to the mantle cavity The brown diges-tive gland surrounds the stomach and extends to theend of the visceral mass In fresh and ethanol-pre-served material a network of thick white vessels run-ning through the digestive gland is clearly visibleThese vessels are not visible in formalin-fixedmaterial

The heart and kidney are similar to Crepidula spe-cies The heart and pericardial cavity are visible in thedorsal side of the viscera The pericardial cavity is at

92 R COLLIN


an angle to the anterio-posterior axis and extendsalong the posterior margin of the mantle cavity InCrepidula species the pericardial cavity is orientatedanterior-posteriorly The hollow kidney is located inthe roof of the mantle cavity anterior to the pericardialcavity and posterior to the distal loop of the intestineThe nephrostome opens into the mantle cavity mid-way between the pericardial cavity and the distal loopof the intestine

The cream or yellow gonad is somewhat external tothe digestive gland and covers almost the entire ven-tral side of the visceral mass in females and the ante-rior ventral side in males The seminal vesicle is aconvoluted narrow tube in the right anterior dorsalmargin of the viscera below the mantle cavity andopens into the open-grooved vas deferens The vas def-erens runs to the base of the penis where an opensperm groove runs medially on the ventral side to itsdistal end The thick flattened penis ends bluntly witha very small papilla The penis is usually considerablylonger than the tentacles and often exceeds the ani-malrsquos body length in small males In females the vis-ceral oviduct and gonopericardial duct join at theright anterior dorsal margin of the visceral masswhere the albumen gland extends up into the roof ofthe mantle cavity Several seminal receptacles con-nect to the albumen gland Distal to the seminalreceptacles the two lobes of the capsule gland con-verge and open directly into the mantle cavitythrough the genital pore The female genital papilla isabsent All species described here show evidence ofprotandry

The nerve ring is located at the posterior margin ofthe neck just anterior to the visceral mass and com-pletely embedded in the salivary glands The nervering is the same as in C fornicata (Werner amp Grell1950) A pair of buccal ganglia are located against thedorsal medial margin of the buccal mass

Radula the taenoioglossate radula (Fig 10) is similarto that of other calyptraeids In Crepidula the majorcusps are straight-sided (eg Collin 2000a) producinga dagger-shaped or triangular cusps In Bostrycapulusthe sides of the major cusps on the rachidian and lat-eral teeth are sinuous The minor cusps on all teethare more appressed to the body of the tooth than inother species The number of denticles on each toothvaries significantly among rows within an individualand among individuals (Table 3)

Development the transparent thin-walled egg cap-sules of Bostrycapulus species are typical of all calyp-traeids The stalks are wide flattened ribbons and notthread-like as in some species The female broods thecapsules between the neck and substrate and propo-dium until hatching Differences in development arediagnostic among species

There are currently eight recognized species in Bos-trycapulus (see Table 4 for summary)

BOSTRYCAPULUS ACULEATUS (GMELIN 1791)SynonymyPatella aculeata Gmelin 1791 3693Crepidula aculeata - Lamarck 1822 25 Reeve 1859

Sowerby 1883 [in part] 67 sp 9 figs 124 125Sowerby 1887 [in part] 67 figs 39 40 Parodiz1939 [in part] 695 Hoagland 1977 [in part] 364Collin 2003a 541ndash593 Collin 2003b 618ndash640

C intorta var Say 1822 227 [in part]C costata Morton 1829 115 pl 7 figs 2 3 Maryland

Tertiary [non C costata Sowerby 1824 necC costata Deshayes 1830]

C spinosa Conrad 1843 307 Miocene VirginiaC ponderosa H C Lea 1846 249 Virginia TertiaryCrypta aculeata - Moumlrch 1877 93ndash123Bostrycapulus aculeatus - Olsson amp Harbison 1953

[in part] 280 Simone 2002 [in part] 18

Original description lsquoPatella aculeata Shell ovalbrown with prickly striae crown recurved ChemnConch 10 tab 168 624 1625 Da Costa Conch tab 6fig 1 Elements t 2 f 2 Favann Conch 1 tab 4 fig 3Walch Naturs 10 tab 1 fig 5 2 Inhabits AmericanIslands resembles the last shell small chestnut orwhite with longitudinal striae lip white dividing thecavity into equal partsrsquo

Fate of original type material the types ofB aculeatus have previously been referred to as lsquolostrsquo(Hoagland 1977) Fates of most of the shells figured inthe works referred to by Gmelin are unknown How-ever the material Chemnitz cited as lsquoEx Museo Nos-trorsquo was sold at public auction and the cataloguelsquoEnumeratio Systematica Conchyliorum beat J HChemnitziirsquo by Havniae 1802 lists Patella aculeata asnumber 1144 (Martynov 2002) A shell with the num-ber 1144 attached to it and matching the figure inChemnitz is housed in the Zoological Museum in StPetersburg Russia There are two other shells in thelot with the figured specimen and notes in the marginof the auction catalogue in St Petersburg mention1144 as containing three shells (Martynov 2002)Specimens of Patella aculeata described by Favannefrom the Cabinet Royal cannot be found in theMuseum National drsquoHistoire Naturelle (P Bouchetpers comm) and C aculeata attributable to da Costaare not in the Natural History London (pers observand D Reid pers comm) Finally inquiries aboutmaterial of C aculeata that may be attributable to anyof these four authors suggests that possible types donot exist in London Paris Leiden Berlin HamburgVienna Copenhagen Frankfurt or Stockholm It istherefore probable that the shell in St Petersburg fig-



ured by Chemnitz is the only remaining type ofB aculeatus

Original type locality Gmelin states the habitat ofB aculeatus to be lsquoIslands of the Americasrsquo This ismost likely following lsquoWestindischenrsquo from Chemnitz

Diagnosis This species can be distinguished fromother Bostrycapulus species by features of develop-ment and mitochondrial DNA sequences Develop-ment is direct from large 380 mm eggs Embryosdevelop characteristic larval features but reabsorbthem prior to hatching The globose protoconch is900 mm in diameter and has less than a single whorlDiagnostic DNA sequence differences distinguishingB aculeatus from all other Bostrycapulus species arein the following positions in the COI sequences sub-mitted to GenBank (position 1 = position 1537 of theDrosophila yakuba mitochondrial genome GenBankX03240) 28 (c) 33 (g) 186 (g) 282 (t) 468 (g)511(c)

Distribution the known distribution of this speciesincludes both coasts of Florida the Florida KeysYucatan the Bahamas and probably the northernCaribbean Sea Shells from as far north as NorthCarolina also probably belong to this speciesalthough this has not been verified by examination ofdevelopment or DNA sequence data It is common onrocks and debris in the shallow subtidal zone and canalso be found on the carapaces of horseshoe crabsRanges to a depth of at least 60 m

DescriptionShell as described for all Bostrycapulus speciesabove Maximum length = 30 mm

Protoconch globose comprising a single whorl c900 mm across No sculpture is retained in materialavailable from juvenile shells The protoconchndashteleo-conch boundary is not distinct (Fig 5H)

Anatomy as described for all Bostrycapulus sppabove

Radula as described for all Bostrycapulus spp above(Fig 10)

Development the egg capsules of B aculeatus are typ-ical of all calyptraeids The stalks are wide flattenedribbons and not thread-like as in some other speciesThe 20ndash30 large yolky eggs per capsule all developdirectly into crawling juveniles Embryos develop asmall but distinct velum an operculum (Fig 8B) asmall round yolk-free head vesicle and a single roundembryonic kidney on each side The velum and tenta-cles have a few cream spots and a dark stripe developsalong the mid-line of the foot late in development

(Fig 8B) Prior to hatching the shell begins to turnbrown and the granular sculpture can be seen clearlywith a dissecting microscope Despite the relativelylarge velum excapsulated embryos are never able toswim free of the bottom of the container Hoagland(1986) reports an egg size of 380 mm and a hatchingsize of 840 mm I found an egg diameter of 378 mm(SD = 9 mm N = 11) for a single female from Lido KeyFlorida

Notes the type locality lsquoislands of the Americasrsquo issomewhat vague but most likely refers to a locality inthe northern Caribbean It is possible that Bostry-capulus from the southern Caribbean is a distinctspecies from the species described here asB aculeatus (Gmelin 1791) I have been unable tofind Bostrycapulus in the Caribbean surroundingPanama Cayman Islands or Trinidad despite find-ing ostensibly appropriate habitat If an additionalCaribbean species is discovered nomenclatural sta-bility would benefit from the description of the south-ern species as new

Observations of embryos are limited because virtu-ally all egg capsules collected in Lido Key Florida in1997 contained nothing but bacterially infected fluidHowever many of those collected in 2003 developednormally Animals are often solitary or form pairsthey do not form large stacks Fossil shells with thismorphology date from the Miocene in Florida (Hoag-land 1977)

BOSTRYCAPULUS GRAVISPINOSUS (KURODA amp HABE 1950)

SynonymyCrepidula gravispinosa Kuroda amp Habe 1950 30 Col-

lin 2003a 541ndash593 Collin 2003b 618ndash640Crepidula aculeata - Taki 1938 [in part] 145 Par-

odiz 1939 [in part] 695 Hoagland 1977 [in part]364

Original description lsquoC gravispinosa n sp for Crep-idula aculeata (not Gmelin) Illust Encyclop FaunaJapan Rev Edit p 1140 textfig 239 1947rsquo The fig-ured referred to is the same as that in the 1927 editionof the Illustrated Encyclopedia of Japanese Fauna butthe text differs

Fate of original type material material illustrated inthe Illustrated Encyclopedia of Japanese Fauna gen-erally belonged to Kurodarsquos personal collection whichis currently housed in Nishinomiya No shell match-ing the figure can be found in this collection (P Cal-lomon pers comm) although it does contain twoshells of B gravispinosus collected from Akune in1949 (P Callomon pers comm) It is also possiblethat the figured shell was from Shintaro Hirasersquos col-

94 R COLLIN


lection or that of his father in which case it waseither taken to Tokyo University or may haveremained in the main Hirase collection which is nowin the Kyoto University Museum (P Callomon perscomm) Much of the former collection was destroyedduring World War II and the figured shell cannot befound there (R Ueshima pers comm) It is thereforelikely that the type material figured in the encyclope-dia is lost

Type locality Hirado Is Nagasaki Prefecture West-ern Kyushu

Diagnosis and description the shell morphology andanatomy of B gravispinosus are the same as otherspecies of Bostrycapulus All specimens available tome are smaller (maximum length is 20 mm) thanB aculeatus The protoconchs retain radial rows offine granular sculpture (Fig 5D) Development isdirect apparently without nurse eggs (Ishiki 1936Amio 1963) although the egg size of 200 mm citedby Amio is too small to produce large juveniles with-out some kind of extraembryonic nutrition The pro-toconchs from Minabe Wakayama Prefecture show amorphology typical of direct development from largeeggs and an apparent hatching size of about 1 mmHatching size is given as 1000 mm by Ishiki (1936)and as 1200 mm by Amio (1963) Since only a singleCOI sequence is available it is difficult to evaluatethe diagnostic differences However apparent diag-nostic DNA sequence differences distinguishingB gravispinosus from all other Bostrycapulus spe-cies are in the following positions in the COIsequences submitted to GenBank (position1 = position 1537 of the D yakuba mitochondrialgenome GenBank X03240) 18(g) 51 (g) 138 (g)175 (c) 296 (c) 340 (t)

Distribution Japan South of Boso Peninsula andwest of Noto Peninsula to the Amami Islands (Taki1938)

Notes fossils occur in Japan in the Tertiary (Hoag-land 1977) The apparent conflict between the egg sizeand hatching size data reported by Ishiki (1936) andAmio (1963) could be explained if there were two Jap-anese species that differed in development Unfortu-nately only a single broken specimen was available forDNA sequencing and the protoconchs were not pre-served on most of the available shells so this possibil-ity cannot be ruled out If multiple species are presentin Japan either historically or due to recent introduc-tions the nomenclatural stability of B gravispinosuswould benefit from the designation of a neotype thatretains either developmental or DNA characters thatcan be used to unambiguously distinguish it from theother species in the Bostrycapulus

BOSTRYCAPULUS CALYPTRAEFORMIS (DESHAYES 1830)

SynonymyCalyptraea echinus Broderip 1834 39 Broderip

1835 203 pl 29 fig 1 Isla Lobos Peru 3 syntypesBMNH 1975113 Hoagland 1986 173ndash183

Calyptraea hystrix Broderip 1834 39 Broderip 1835203 pl 29 fig 2 Isla Lobos Peru 3 syntypesBMNH 1966629

Crepidula aculeata - Parodiz 1939 [in part] 695Hoagland 1977 [in part] 364

Bostrycapulus aculeatus - Olsson amp Harbison 1953[in part] 280 Simone 2002 [in part] 18

Crepidula cf aculeata - sp 2 Collin 2003b 618ndash640

C cf aculeata - Panama Collin 2003a 541ndash593

Original description lsquoC testacirc ovato-rotundatacirc gib-bosacirc rufescente longitudinaliter striatacirc strius rugo-sis ad marginem evanescentibus apice obliquospiratorsquo

Type material two syntypes in the Paris museum(Hoagland 1983 P Bouchet 2001 pers comm) One isfigured in Hoagland (1983)

Type locality Peru () Deshayes (1830) supposed thatthe types came from Peru because they were boughtwith shells of other Peruvian species

Diagnosis the shell morphology and anatomy ofB calyptraeformis do not differ from those ofB aculeatus as described above B calytraeformis canbe distinguished from the other species of Bostrycapu-lus by the presence of planktotrophic developmentand a smooth protoconch with 15 whorls (Fig 5)Diagnostic DNA sequence differences distinguishingB calyptraeformis from all other Bostrycapulusspecies are in the following positions in the COIsequences submitted to GenBank (position1 = position 1537 of the D yakuba mitochondrialgenome GenBank X03240) 39 (g) 42 (c) 57 (g) 69(a) 75 (c) 171 (c) 259 (t) 282 (g) 321 (a) 354 (g) 387(c) 402 (c) 441 (c) 462 (g) 486 (c) 582 (c)

Distribution northern Peru to the Pacific coast ofeastern Panama and the Perlas Islands but notextending into the Gulf of Chiriqui This species alsooccurs in Hawaii where it is probably introduced andit may have been recently introduced into Guam Thisspecies can reach densities of greater than 1000 indi-viduals per square meter in the intertidal zone of Pan-ama (unpubl data) and occurs to depths of at least50 m

Description shell morphology and anatomy of thisspecies differ from B aculeatus only in protoconchmorphology (Fig 5B E) Development is plank-



totrophic Animals from Panama produce small180 mm eggs (Hoagland 1986) and hatch at a length of345 mm (Collin 2003c) At hatching the larval shell iscovered with fine spines or periostracal hairs that arevisible under a compound microscope Animals fromHawaii hatch at 320 mm (Bell 1993) The veliger lar-vae have a black intestine and two small red stripesin the food groove along the anteriolateral and poste-riolateral corners of the velum (Fig 8B) There are nopigment spots on the foot or velum Larvae from Pan-ama settle in culture starting at a shell length of 700ndash800 mm (pers observ Collin 2003c) Animals fromnorthern Peru (Mancora Zorritos and Paita) alsohave planktotrophic development but more detailedobservations are not available This is the only knownspecies of Bostrycapulus with planktonic larvae

Notes the type of this species is from Peru and thedescription presented here is based on material fromthe north coast of mainland Peru supplemented withobservations of material from Panama and Hawaii Asdiagnostic material from Isla Lobos is not currentlyavailable the synonymy of C calyptraeformis withC echinus and C hysterix has yet to be rigorouslydemonstrated The genetic differentiation between thesamples from Peru and Panama and Hawaii is almostas great as the differentiation among other siblingCrepidula species (eg Collin 2000a 2001) suggestingthat these may be two distinct species Because theavailable data are insufficient to unambiguouslydetermine the status of these populations and I amaware of no differentiation other than the DNAsequences I have chosen to conservatively place themall in B calyptraeformis until more information isavailable

BOSTRYCAPULUS CF TEGULICIUS

SynonymyCrepidula aculeata - Hoagland 1977 [in part] 364

Hoagland 1983 [in part]Crepidula cf tegulicia - Collin 2003a 541ndash593 Col-

lin 2003b 618ndash640

Original description (of Crypta tegulicia Rochebrune1883) lsquoTesta subovata crassiuscula irregularioblique curvata extus albida concentrice striata etsquamis minutis teguliformibus subdistantibus orni-ata intus nitide castaneo violacea lamella opalina admedio et ad latus subemarginata Long 0019 Lat0014rsquo

Type two syntypes of B tegulicius are in the Parismuseum (Hoagland 1983 P Bouchet 2001 perscomm) One is figured in Hoagland (1983)

Type locality lsquoDakar Joalles Pointe de Cap VertrsquoSenegal

Diagnosis and description B cf tegulicius can be dis-tinguished from other species in the B aculeatus spe-cies complex by the large globose protoconch anddistinct COI sequence Material with other potentiallydiagnostic features is not currently available Diag-nostic DNA sequence differences are difficult to deter-mine but the single available sequence distinguishingB cf tegulicius from all other Bostrycapulus species isin the following positions in the COI sequences sub-mitted to GenBank (position 1 = position 1537 of theD yakuba mitochondrial genome GenBank X03240)178 (a) 268 (t) 282 (c) 339 (g) 492 (a) 583 (a)

Distribution Cape Verde Islands The extent of thedistribution along the west coast of Africa is unknown

Notes B tegulicius was originally described fromSenegal As diagnostic material from this country isnot currently available the identity of the Cape Ver-dian material described here cannot be unambigu-ously assigned to a new species It is quite possiblethat they are different species since the Cape Verdiananimals have direct development (and therefore pre-sumably limited dispersal) and many Cape Verdianspecies are endemic to these islands If animals fromSenegal and Cape Verde are demonstrated to belong todifferent species the name B tegulicius should beapplied to material from mainland Africa while thespecies from Cape Verde should be given a new name

BOSTRYCAPULUS PRITZKERI SP NOVSynonymyCrepidula aculeata - Parodiz 1939 [in part] 695

Hoagland 1977 [in part] 364Bostrycapulus aculeatus - Olsson amp Harbison 1953

280 Simone 2002 [in part] 18Crepidula cf aculeata - Australia Collin 2003a 541ndash

593Crepidula cf aculeata - Sydney Collin 2003b 618ndash

640

Holotype Australian Museum C400000 shelland ethanol-preserved soft parts Shell illustratedin Figure 11 length = 148 mm width = 118 mmheight = 41 mm Frozen tissue of this specimenFMNH 282361

Type locality Edwards Reef Sydney Australia33infin51centS 151infin13centE Low intertidal zone on rocks

Other material from type locality FMNH 282302(paratypes)

Diagnosis B pritzkeri can be distinguished from theother species in Bostrycapulus by its large globoseprotoconch and direct development from large eggsthat produce embryos lacking the larval featurespresent in other direct developing species of Bostry-

96 R COLLIN


capulus Diagnostic DNA sequence differences distin-guishing B pritzkeri from all other Bostrycapulusspecies are in the following positions in the COIsequences submitted to GenBank (position1 = position 1537 of the D yakuba mitochondrialgeneome GenBank X03240) 183 (c) 256 (c) 315 (c)360 (c) 395 (c) 417 (g) 444 (g) 471 (g) 477 (c)

Distribution south-eastern Australia The AustralianNational Museum contains shells with this morphol-ogy from the coast of New South Wales and Queen-sland but the species identity of the latter materialneeds to be verified with additional observations oflive material and genetic data

Description shell morphology and anatomy ofB pritzkeri are the same as B aculeatus except thatthe yellow or cream pigment makes a pattern of radialstripes or narrow triangles extending from the edge ofthe foot to the mantle edge Direct development pro-ceeds from large ~545 mm eggs Intracapsularembryos retain few larval characters The velum isreduced to a simple ridge at the base of the tentacle

(Fig 6) and the food groove is absent There is no oper-culum and the head vesicle is medium-sized and freeof yolk The embryonic shell has widely spaced rows ofgranular sculpture which are not visible on the proto-conchs examined with SEM The very large egg sizeresults in the most globose and least coiled of any Bos-trycapulus protoconch (Fig 5A)

Etymology the name pritzkeri is in honour of R Pritz-ker president of the Pritzker Foundation The Foun-dationrsquos support of the Pritzker Laboratory ofMolecular Systematics and Evolution at the FieldMuseum made this work possible

BOSTRYCAPULUS ODITES SP NOVSynonymyCrepidula aculeata - Parodiz 1939 [in part] 695

Hoagland 1977 [in part] 364Crepidula aculeata var fortis - Parodiz 1939 696Bostrycapulus aculeatus - Olsson amp Harbison 1953


Figure 11 The shells of the holotypes of the four new species A Bostrycapulus latebrus (FMNH 282358) B B odites(Natal Museum V9447T1783) C B pritzkeri (Australian Museum C400000) D B urraca (ANSP 412178) Scalebar = 10 mm

A B C D




Crepidula cf aculeata - South Africa Collin 2003a541ndash593

Crepidula cf aculeata - Argentina Collin 2003a541ndash593

Crepidula cf aculeata - Brazil Collin 2003a 541ndash593

Holotype Natal Museum V9447T1783 shell andethanol-preserved soft parts Shell illustrated inFigure 11 length 193 mm width 156 mm height72 mm Frozen tissue of this specimen FMNH282360

Other live-collected material from the type localityFMNH 282277 (paratype) BM20010453

Other live-collected material examined FMNH282297 ANSP A19744 BM20010456 FMNH 282350FMNH 282368

Type locality Wooleys Pool Muizenburg Cape Prov-ince South Africa Low intertidal zone in rock crev-ices co-occurring with Crepipatella capensis

Diagnosis B odites differs from the other species inthe B aculeatus species complex in exhibiting directdevelopment from small eggs which consume nurseeggs The protoconch is unsculptured and retainsirregular growth lines (Figs 5F 4I) Adult morpholog-ical characters are as described above for B aculeatusDiagnostic DNA sequence differences distinguishingB odites from all other Bostrycapulus species are inthe following positions in the COI sequences submit-ted to GenBank (position 1 = position 1537 of theD yakuba mitochondrial genome GenBank X03240)24 (c) 36 (g) 141 (c) 220 (t) 234 (c) 279 (g) 354 (t)438 (c) 486 (a) 552 (t)

Distribution and habitat the Atlantic coast of SouthAmerica from Satildeo Paulo Brazil to Puerto MadrynArgentina as well as the south coast of South Africafrom Cape Town to Port Elizabeth and north to north-ern Natal (Natal Museum) Material examined herewas collected from rocks intertidally in South Africaand Brazil and intertidally from rocks and subtidallyfrom the shells of pen-shells and oysters in ArgentinaThis species occurs to depths of at least 40 m

Description shell morphology and anatomy are thesame as B aculeatus with the exception of the proto-conch The 1 mm diameter protoconch is smooth withirregular growth lines towards the aperture (Figs 5F4I) The indistinct protoconchndashteleoconch boundaryoccurs after slightly more than a single whorl iscompleted

Observations of development are available for ani-mals from Argentina and Cape Town but only the

early stages were collected Eggs from Argentiniananimals are 197 mm in diameter All eggs in a capsulebegin to develop synchronously and gastrulationincludes invagination Gastrulas look similar to thoseof C lingulata (Collin 2000b) After gastrulation thenurse eggs remain spherical with centralized yolk andciliated epithelium After consuming the nurse eggsthe remaining embryos form intracapsular veligerswith a single embryonic kidney on each side a dis-tinct operculum a very small distinct velum with afood groove a small round head vesicle and someblack pigment on the intestine The shells of earlyembryos appear smooth under a dissecting micro-scope Embryos near hatching were not observed inOctober and November in Argentina or December inSouth Africa I observed the development of a fewbroods of South African animals It appears that theembryos begin to consume the nurse eggs slightly ear-lier in development than those from Argentina andthat the larval features are therefore slightly less welldeveloped relative to embryo size Maximumlength = 30 mm

Etymology odites is a Greek noun meaning travellerThis name refers to the large geographical distribu-tion this species has attained despite its directdevelopment

BOSTRYCAPULUS LATEBRUS SP NOVSynonymyCrepidula aculeata - Hoagland 1977 [in part] 364Crepidula cf aculeata - Mexico Collin 2003a 541ndash

593 Collin 2003b 618ndash640

Holotype FMNH 282358 shell and ethanol-preservedsoft parts Shell illustrated in Figure 11 length =150 mm width = 119 mm height = 41 mm Frozentissue is also deposited at the FMNH under the samelot number

Type locality just north of La Paz Baja CaliforniaSur Mexico along the coast of Ensenada La Paz nearEl Comitaacuten Collected from rocks in the low intertidalzone

Other material from the type locality FMNH 282193(paratype) FMNH 282194

Diagnosis B latebrus can be distinguished fromother species of Bostrycapulus by DNA sequence dataand by its direct development from large eggswith embryos that retain larval features (unlikeB pritzkeri) The shell morphology and anatomy ofB latebrus do not differ from that described above forB aculeatus Diagnostic DNA sequence differencesdistinguishing B latebrus from all other Bostrycapu-lus species are in the following positions in the COI

98 R COLLIN


sequences submitted to GenBank (position1 = position 1537 of the D yakuba mitochondrialgenome GenBank X03240) 3 (g) 108 (c) 144 (g) 192(g) 243 (a) 270 (c) 306 (g) 327 (g) 423 (c) 522 (t)

Distribution material whose identity can be verifiedas B latebrus has only been collected near La PazMexico Shells that may be from this species occurcommonly along the Pacific coast of Baja Californiaand have been reported from as far north as southernCalifornia However observations of development andDNA data are necessary before their identity can beverified

Description shell morphology and anatomy are thesame as for B aculeatus although the shells of thelive-collected material were all smaller than largeexamples of B aculeatus and B odites The protoconchdistinguishes this species from B calyptraeformis andB odites and B pritzkeri but cannot be used toclearly distinguish it from the other species of Bostry-capulus B latebrus has direct development from eggswith a diameter of 488 mm The embryos develop intointracapsular lsquoveligersrsquo with a very small but distinctun-pigmented velum a small round head vesicle and asingle embryonic kidney on each side An operculum ispresent but is lost before hatching Embryonic shellsculpture consists of widely spaced rows of fine gran-ules similar to the larval sculpture of C lingulata(Collin 2000b) Embryos hatch as crawling juvenilesMaximum shell length 16 mm (N = 20)

Etymology The species name latebrus is Latin mean-ing lsquohiddenrsquo or lsquoobscurersquo referring to both the difficultyof distinguishing this from the other species of Bostry-capulus and also to the fact that shells are often soencrusted with epibionts that they are effectively hid-den in the field

Notes C californica Tryon 1886 is a nomen nudumHowever it may possibly have been applied to thisspecies in the previous literature Fossil shells withsimilar morphology occur in the Pliocene andPleistocene of California USA and Baja CaliforniaMexico

BOSTRYCAPULUS URRACA SP NOV

Holotype ANSP 412178 Figure 11D length =154 mm width = 131 mm height = 57 mm

Paratypes ANSP 412179 (two animals from the typelocality)

Type locality Isla Parida Gulf of Chiriqui Panama8infin5458centN 82infin18671centW

Other live material from type locality Isla ParidaGulf of Chiriqui Panama FMNH 306483

Diagnosis B urraca can be distinguished from otherspecies of Bostrycapulus by a combination of the fol-lowing It has a large globose protoconch and directdevelopment that retains most of the larval featuresDiagnostic DNA sequence differences distinguishingB urraca from all other Bostrycapulus species are inthe following positions in the COI sequences submit-ted to GenBank (position 1 = position 1537 of theD yakuba mitochondrial genome GenBank X03240)261 (t) 285 (g) 309 (g) 375 (t) 474 (c) 495 (a) 588 (t)

Distribution material whose identity has be verifiedas B urraca has been collected in Panama from theGulf of Chiriqui Isla Coiba the Azuero Peninsula andthe Perlas Archipelago In El Salvador it has been col-lected from the Gulf of Fonseca This species occursfrom the intertidal zone to at least 50 m and can occurin densities up to several hundred per square meter inthe intertidal zone

Description shell morphology and anatomy are thesame as B aculeatus Although B urraca often hasmore distinct spination than the other species ofBostrycapulus sequences of particularly spiny andsmooth animals from the Gulf of Chiriqui and Bay ofPanama showed that this is intraspecific variationand cannot be used to distinguish between these twospecies This species has direct development from eggswith a diameter of 360 mm (SD = 72 N = 57) and witha hatching size of 888 mm (SD = 70 N = 75) Theembryos develop and coiled shell an operculum andpaired embryonic kidneys (Fig 7) The velum is lim-ited to a ring of ciliated cells around the head and doesnot have a well-defined food-groove (Fig 7)

Etymology The species name urraca is a noun inapposition The name honours the RV Urraca theSmithsonian Tropical Research Institutersquos researchvessel which was used to collect samples of this spe-cies Urraca was the name of a Guaymi chief whofought bravely against the Spanish in Panama

ACKNOWLEDGEMENTS

I thank G Branch N Ciocco M Byrne C Caacuteceres JLeal H Lessios R Gonzales and S Valle for hostingme in their laboratories A Indacochea J Troncoso FRubio and E Rolaacuten for accompanying me in the fieldthe crew of RV Urraca for assistance with field sam-pling the curators and collection managers of USNMBMNH CAS ANSP MCZ ZMUC LACM FMNHAMS and NMP for access to samples in their careB Strack for assistance with the scanning electronmicroscope and P Callomon for vigorous discussion ofC gravispinosa M Hadfield R Kilburn L SimoneG Paulay C Redfern R Robertson F Rodriguez KNoda and M Katoh provided additional material I am



especially grateful for taxonomic assistance and sug-gestions from R Kilburn D Reid P Callomon and AWareacuten and for A Martynovrsquos effort to find the type ofC aculeata R Robertson P Callomon A Wareacuten andJ Voight commented on previous versions of themanuscript Sequencing was carried out in thePritzker Laboratory for Molecular Systematics andEvolution operated with support from the PritzkerFoundation Financial support for this research wasprovided by the National Science Foundation (Disser-tation Improvement Grant DEB 9972555)

REFERENCES

Amio M 1963 A comparative embryology of marine gastro-pods which ecological emphasis Journal of ShimonosekiCollege Fisheries 12 229ndash253

Bell JL 1993 Feeding and growth of prosobranch veligersPhD Dissertation University of Hawaii

Bouchet P 1989 A review of poecilogony in gastropods Jour-nal of Molluscan Studies 55 67ndash78

Bowen BW Bass AL Rocha LA Grant WS RobertsonDR 2001 Phylogeography of the trumpetfishes (Aulosto-mus) ring species complex on a global scale Evolution 551029ndash1039

Broderip WJ 1834 Characters of new genera and species ofMollusca and Conchifera collected by Mr Cuming Descrip-tions of new species of Calyptraeidae Proceedings of the Zoo-logical Society of London 2 35ndash40

Colborn J Crabtree RE Shaklee JB Pfeiler E BowenBW 2001 The evolutionary enigma of bonefishes (Albulaspp) Cryptic species an ancient separation in a globally dis-tributed shorefish Evolution 55 807ndash820

Colbourne JK Crease TJ Weider LJ Hebert PDNDufresne F Hobaek A 1998 Phylogenetics and evolu-tion of a circumarctic species complex (Cladocera Daphniapulex) Biological Journal of the Linnean Society 65 347ndash365

Colbourne JK Hebert PDN 1996 The systematics of NorthAmerican Daphnia (Crustacea Anomopoda) a molecularphylogenetic approach Philosophical Transactions of theRoyal Society of London B 351 349ndash360

Coles SL Defelice RC Eldredge LG Carlton JT 2000Historical and recent introductions of non-indigenousmarine species into Pearl Harbor Oahu Hawaii IslandsMarine Biology 135 147ndash158

Collin R 2000a Phylogeny of the Crepidula plana (Gas-tropoda Calyptraeidae) cryptic species complex in NorthAmerica Canadian Journal of Zoology 78 1500ndash1514

Collin R 2000b Sex change reproduction and development ofCrepidula adunca and C lingulata (Gastropoda Calyp-traeidae) Veliger 43 24ndash33

Collin R 2001 Effects of mode of development on phylogoeg-raphy and population structure of North Atlantic Crepidula(Gastropoda Calyptraeidae) Molecular Ecology 10 2249ndash2262

Collin R 2002 Another last word on Crepidula convexa and adescription of C ustulatulina sp nov (Gastropoda Calyp-traeidae) from the Gulf of Mexico Bulletin of Marine Science70 (1) 177ndash184

Collin R 2003a The utility of morphological characters ingastropod phylogenetics An example from the Calyp-traeidae Biological Journal of the Linnean Society 78 541ndash593

Collin R 2003b Phylogenetic relationships amongcalyptraeid gastropods and their implications for thebiogeography of speciation Systematic Biology 52 (5) 618ndash640

Collin R 2003c Worldwide patterns in mode of developmentin calyptraeid gastropods Marine Ecology Progress Series247 103ndash122

Conrad TA 1843 Descriptions of a new genus and of twenty-nine new Miocene and one Eocene fossil shells of the UnitedStates Proceedings of the Academy of Natural Sciences ofPhiladelphia 1 305ndash311

Deshayes GP 1830 Encyclopedie Methodique des Vers 2 (2)24ndash28

Fischer von Waldheim G 1807 Veacutegeacutetaux et AnimauxMuseum Demidoff ou Catalogue des curiositeacutes de la nature etde lrsquoArt donneacutees a lrsquoUniversiteacute imperiale de Moscou par M deDemidoff 3 Moscow 1ndash330

Folmer O Black M Hoeh W Lutz R Vrijenhoek R 1994DNA primers for amplification of mitochondrial cytochromec oxidase subunit I from diverse metazoan invertebratesMolecular Marine Biology and Biotechnology 3 (5) 294ndash299

Gallardo CS 1979 Especies gemelas del geacutenero Crepidula enla costa de Chile una redescripcioacuten de C dilatata Lamarcky descripcioacuten de C fecunda n sp Studies on NeotropicalFauna and Environment 14 (4) 216ndash227

Geller JB 1999 Decline of a native mussel masked by siblingspecies invasion Conservation Biology 13 661ndash664

Geller JB Walton ED Grosholz ED Ruiz GM 1997 Cryp-tic invasions of the crab Carcinus detected by molecular phy-logeography Molecular Ecology 6 901ndash906

Gmelin JF 1791 Systema Naturae 13th ed Vol1 (6) 3021ndash4120

Goacutemez A Serra M Carvalho GR Kunt DH 2002 Specia-tion in ancient cryptic species complexes evidence from themolecular phylogeny of Brachionus plicatilis (Rotifera) Evo-lution 56 1431ndash1444

Helmuth B Veit RR Holberton R 1994 Long-distancedispersal of a subantarctic brooding bivalve (Gaimardiatrapesina) by kelp-rafting Marine Biology 120 421ndash426

Hoagland KE 1977 Systematic review of fossil and recentCrepidula and discussion of evolution of the CalyptraeidaeMalacologia 16 (2) 353ndash420

Hoagland KE 1983 Notes on type specimens of Crepidula(Prosobranchia Calyptraeidae) in the Museacuteum NationaldrsquoHistoire Naturelle Paris Proceedings of the Academy ofNatural Sciences of Philadelphia 135 1ndash8

Hoagland KE 1984 Use of molecular genetics to distinguishspecies of the gastropod genus Crepidula (ProsobranchiaCalyptraeidae) Malacologia 25 (2) 607ndash628

100 R COLLIN


Hoagland KE 1986 Patterns of encapsulation and broodingin the Calyptraeidae (Prosobranchia Mesogastropoda)American Malacological Bulletin 4 (2) 173ndash183

Hoagland KE Robertson RR 1988 An assessment ofpoecilogony in marine invertebrates phenomenon or fan-tasy Biological Bulletin 174 109ndash125

Huelsenbeck JP 2000 Mrbayes Bayesian inference of phy-logeny Distributed by the author Dept Biology Universityof Rochester

Huelsenbeck JP Ronquist F 2001 Mrbayes 2 0 Bayesianinference of phylogeny Distributed by the author Dept Biol-ogy University of Rochester and Dept Biology University ofUppsala

Ishiki H 1936 Sex-changes in Japanese slipper limpetsCrepidula aculeata and Crepidula walshi Journal of Scienceof Hiroshima University Series B 4 91ndash99

Ivanov DL Kantor YI Sysoev AV Egorov RV 1993 Typespecimens of molluscs described by G Fischer von Waldheimin 1807 Apex 8 (3) 71ndash83

Kleinsteuber H 1913 Die Anatomie von Trochita Calyp-traea und Janacus Fauna Chilensis Zoologische Jahr-buumlcher Supplement 8 (4) 385ndash476

Knowlton N 1993 Sibling species in the sea Annual Reviewof Ecology and Systematics 24 189ndash216

Knowlton N Weigt LA 1998 New dates and new rates fordivergence across the Isthmus of Panama Proceedings of theRoyal Society of London B 265 2257ndash2263

Kuroda T Habe T 1950 Nomenclatural notes Illustratedcatalogue of Japanese shells 4 30

Lea HC 1846 Description of some new fossil shells from theTertiary of Petersburg Virginia Transactions of the Ameri-can Philosophical Society Series 2 9 229ndash274

Lessios HA Kessing BD Pearse JS 2001 Populationstructure and speciation in tropical seas global phy-logeography of the sea urchin Diadema Evolution 55 955ndash975

Lessios HA Kessing BD Robertson DR Paulay G 1999Phylogeography of the pantropical sea urchin Eucidaris inrelation to land barriers and ocean currents Evolution 53806ndash817

Leviton AE Gibbs RH Heal E Dawson CE 1985 Stan-dards in herpetology and ichthyology Part I Standardsymbolic codes for institutional resource collections inherpetology and ichthyology Copeia 1985 (3) 802ndash832

Marko PB 2004 lsquoWhatrsquos larvae got to do with itrsquo Disparatepatterns of post-glacial population structure in two benthicmarine gastropods with identical dispersal potential Molec-ular Ecology 13 597ndash611

Martynov AV 2002 The shell collection of J H Chemnitz inthe Zoological Institute St Petersburg Ruthentica 12 (1)1ndash18

Morton SG 1829 Description of two new species of shells ofthe genera Scaphites and Crepidula Journal of the Academyof Natural Sciences of Philadelphia 6 107ndash119

Murphy PG 1978 Collisella austrodigitalis sp nov A siblingspecies of limpet (Acmaeidae) discovered by electrophoresisBiological Bulletin 155 193ndash206

Muss A Robertson DR Stepien CA Wirtz P Bowen BW

2001 Phylogeography of Ophioblennius The role of oceancurrents and geography in reef fish evolution Evolution 55561ndash572

Olsson AA Harbison A 1953 Pliocene Mollusca of southernFlorida Academy of Natural Sciences of Philadelphia Mono-graph 8 1ndash457

Palumbi SR 1996 Nucleic acids II the polymerase chainreaction In Hillis DM Moritz C Mable BK eds Molecularsystematics Sunderland MA Sinauer 205ndash248

Parodiz JJ 1939 Las especies de Crepidula de las costasArgentinas Physis 17 685ndash709

Posada D Crandell KA 1998 Modeltest testing the modelof DNA substitution Bioinformatics 14 817ndash818

Posada D Crandell KA 2001 Selecting the best-fit model ofnucleotide substitution Systematic Biology 50 580ndash601

Quoy JRC Gaimard JP 1832ndash33 Voyage de lrsquoAstrolabeZoologie Mollusques 3 Paris

Reeve LA 1859 Conchologia Iconica or Illustrations of theShells of Molluscous Animals 11 London

Rocha-Olivares A Fleeger JW Foltz DW 2001 Decouplingof molecular and morphological evolution in deep lineages ofa meiobenthic harpacticoid copepod Molecular Biology andEvolution 18 1088ndash1102

de Rochebrune AT 1883 Diagnosis de mollusques nouveauxpropres agrave la Seacuteneacutegambie Bulletin de la Socieacuteteacute Philo-mathique de Paris Seacuterie 7 177ndash182

Say T 1822 An account of the marine shells of the UnitedStates Journal of the Academy of Natural Sciences of Phil-adelphia 2 221ndash227

Simone LRL 2002 Comparative morphological study andphylogeny of representatives of the superfamilies Calyptrae-oidea (including Hipponicoidea) (Mollusca Caenogas-tropoda) Bioto Neotropica 2 (2) httpwwwbiotaneotropicaorgbr

Smith SDA 2002 Kelp rafts in the Southern Ocean GlobalEcology and Biogeography 11 67ndash69

Sowerby GB 1883 Monograph of the family CalyptraeidaeThesaurus Conchyliorum 5 55ndash74

Swofford DL 1998 PAUP phylogenetic analysis using par-simony (and other methods) v 4 Sunderland MA Sinauer

Taki I 1938 Systematic study of Japanese species of Calyp-traeidae Venus 8 136ndash147

Tryon GW 1886 Manual of conchology Academy of NaturalSciences Philadelphia Series 1 (8) 1ndash461

Veacuteliz D Guisado C Winkler F 2001 Morphological repro-ductive and genetic variability among three populations ofCrucibulum quiriquinae (Gastropoda Calyptraeidae) inNorthern Chile Marine Biology 139 527ndash534

Veacuteliz D Winkler F Guisado C 2003 Developmental andgenetic evidence for the existence of three morphologicallycryptic species of Crepidula in northern Chile Marine Biol-ogy 143 131ndash142

Wares JP 2001 Patterns of speciation inferred from mito-chondrial DNA in North American Chthamalus (CirripediaBalanomorpha Chthamaloidea) Molecular Phylogeny andEvolution 18 104ndash116

Waters JM Roy MS 2004 Out of Africa The slow train toAustralasia Systematic Biology 53 18ndash24



Werner B Grell KG 1950 Die Amerikanische Pantof-felschnecke Crepidula fornicata L Eine Anleitung zur Praumlp-aration Jena Gustav Fischer

Williams ST 2000 Species boundaries in the starfish genusLinckia Marine Biology 136 137ndash148

Witt JDS Hebert PDN 2000 Cryptic species diversity andevolution in the amphipod genus Hyalella within central gla-ciated North America a molecular phylogenetic approachCanadian Journal of Fisheries and Aquatic Science 57 687ndash698

76

R COLLIN



2005

144

75ndash101

et al

2001) Careful examination of morphologicallycryptic species often reveals chemical behavioural ordevelopmental differences further supporting theirstatus as distinct species (Knowlton 1993) Such dif-ferences demonstrate that there has been adequatetime for divergence to occur despite the observed mor-phological stasis

Calyptraeid gastropods are one such group wheremorphological characters cannot always be used todiscriminate effectively among species The simplicityand plasticity of calyptraeid shells has led to muchtaxonomic uncertainty and instability in this family(Hoagland 1977 1984 1986 Collin 2000a 2002Veacuteliz

et al

2001 2003) Anatomical features can beused to distinguish among major species groupswithin some genera but are very conservative andoften cannot be used to distinguish between closelyrelated species (Collin 2003a) Genetic and develop-mental features appear to diverge more rapidly thando morphological characters Therefore it is not sur-prising that recent work with the genetics and devel-opment of

Crepidula

and

Crucibulum

has led to therecognition and formal description of several morpho-logically cryptic species (eg Gallardo 1979 Hoag-land 1984 Collin 2000a 2002 Veacuteliz

et al

2001)High-level phylogenetic analyses of calyptraeids

have led to the discovery of a group of eight crypticspecies all of which were most recently ascribed to

Crepidula aculeata

(Gmelin 1791) (Hoagland 1977)

Crepidula aculeata sl

has a distinctive shell shape itis one of the few lsquo

Crepidularsquo

that retains clear tracesof coiling the shelf has a distinctive longitudinalridge and the shell often has numerous spines (Fig 1)The shells are distinct enough to have been attributedto a separate subgenus

Bostrycapulus

Olsson amp Har-bison 1953 which has sometimes been raised togenus level Phylogenetic analyses of calyptraeidsbased on anatomical (70 species Collin 2003a) andmolecular (94 species Collin 2003b) data show thatspecies in the

aculeata

group fall outside

Crepidulas

s

and are more closely related to

Crucibulum

and

Crepipatella

Therefore they should be referred to

Bostrycapulus

In her review of

Crepidula

Hoagland (1977) synon-ymized all the named species with shell characteris-tics that place them in the lsquoaculeatarsquo group with

C aculeata

but noted that it was unusual for a singlespecies without planktonic larvae to have such a widedisjunct geographical distribution After more exten-sive work with development she removed samplesfrom Panama which she called

C echinus

(Broderip1834) from synonymy with

C aculeata

withoutexplaining the change in nomenclature (Hoagland1986) My previous phylogenetic analyses ofcalpytraeids have included individuals of what appearto be several species in this group (labelled as lsquocf

aculeatarsquo in Collin 2003a b) Here I present morpho-logical developmental genetic and biogeographicaldata with the following aims (1) augmenting thedescription of

Bostrycapulus

(2) determining the rela-tionships between the different species within

Bostry-capulus

and (3) clearly delimiting the species withinthe genus

MATERIAL AND METHODS

Locality information for the live-collected specimensthat were examined or sequenced for this study arelisted in Table 1 Vouchers are deposited at the FieldMuseum of Natural History Chicago USA The Nat-ural History Museum London England and theAcademy of Natural Sciences Philadelphia USA Pro-toconchs were obtained from the same populationsexcept for the Japanese animals which were obtainedfrom shells provided by K Noda from MinabeWakayama Prefecture and Cape Verdian animalswhere protoconchs were obtained from shells providedby Emilio Rolaacuten from Rife de Chaves Sal Rei Bay BoaVista Numerous museum lots of mostly dry materialwere examined from FMNH ANSP CAS NMPNMNZ USNM AMS BMNH and IZUA Museumabbreviations follow Leviton

et al

(1985)A 611 base pair fragment of the mitochondrial cyto-

chrome oxidase I (COI) gene and a fragment of mito-chondrial 16S rDNA were sequenced for individualsfrom each locality and deposited in GenBank As thesedata were originally obtained for interspecific phylo-genetic analysis few individuals were sequenced foreach locality and in several cases only a single etha-nol-preserved individual was available for sequencing(eg

B

cf

tegulicius

) DNA was extracted from etha-nol-preserved tissue with Puregene (Gentra Systems)or DNeasy (Quiagen) extraction kits amplified usingReady-To-Go PCR beads (Pharmacia Biotech) andprimers and PCR profile of Folmer

et al

(1994) and16sar

-

16sbr of Palumbi (1996) PCR products weresequenced in both directions with dRhodamine (Per-kin Elmer) or Big Dyes cycle sequencing dye termina-tor kits using the amplification primers and an ABI377 automated sequencer Sequences were alignedusing Sequencher 30 and alignments were adjustedby eye

Phylogenetic analyses were conducted usingPAUP v 4b02 (Swofford 1998) An equal-weightedunrooted parsimony analysis was performed withgaps coded as a fifth character using a heuristicsearch with TBR branch swapping and 1000 randomadditions Bootstrap support for each clade wasassessed based on 1000 bootstrap replicates withTBR branch swapping and ten random additions Iincluded

Crepipatella lingulata

C capensis

and

Cru-cibulum auriculum

three close outgroups of

Bostry-

SYSTEMATICS OF

BOSTRYCAPULUS

77



2005

144

75ndash101

Figure 1

Photographs of (A)



B odites

sp nov


=

10 mm

A

B

78

R COLLIN



2005

144

75ndash101

Tab

le 1

Su

mm

ary

of li

ve-c

olle

cted

mat

eria

l use

d fo

r ob

serv

atio

ns

of d

evel

opm

ent

and

anat

omy

and

for

DN

A s

equ

enci

ng

Abb

revi

atio

ns

BM

SM

Bai

ley-

Mat

thew

sS

hel

l M

use

um

K

LK

C K

L K

aise

r C

olle

ctio

n

Spe

cies

Loc

alit

yM

ode

of d

evel

opm

ent

Vou

cher

nos

G

enba

nk

nos

CO

IG

enba

nk

nos

16S

B a

cule

atu

s

M

ote

Mar

ine

Lab

orat

ory

Lid

o K

ey

Flo

rida

U

SA

27

infin

20

cent

N

82

infin

42

cent

W[

gt

30 a

nim

als]

Dir

ect

(obs

erve

d)A

NS

P A

1974

5F

MN

H 2

8236

5B

M20

0104

55

AY

0617

92 A

Y61

8322

-3A

Y06

1774

Har

bor

Bra

nch

Oce

anog

raph

icIn

stit

ute

F

lori

daU

SA

28

infin

29

cent

N 8

1

infin

20

cent

W [

3 an

imal

s]

Dir

ect

(obs

erve

d)F

MN

H 3

0648

1A

Y61

8317

ndash

Flo

rida

Key

s U

SA

24

infin

40

cent

50

cent

N

82

infin

16

cent

02

cent

W [

2 an

imal

s]D

irec

t (o

bser

ved)

FM

NH

282

284

AY

0617

77ndash

Aba

co B

aham

as 2

6

infin

42

cent

56

cent

N

77

infin

14

cent

33

cent

W [

5 an

imal

s]N

ot o

bser

ved

BM

SM

262

92B

MS

M 2

6293

B

MS

M 2

6294

BM

SM

262

95

AY

6183

46-7

ndash

B g

ravi

spin

osu

s

Ch

ijiw

a N

agas

aki

Japa

n[1

an

imal

]N

ot o

bser

ved

FM

NH

282

336

AY

0617

83A

Y06

1766

B c

alyp

trae

form

is

Pla

ya V

enad

o P

anam

a 8

infin

55

cent

N

79

infin

38

centW [

gt10

0 an

imal

s]P

lan

ktot

roph

ic(o

bser

ved)

FM

NH

282

273

AN

SP

A19

740

BM

2001

0452

AY

0617

86 A

Y61

8328

AY

6183

34-4

0

AY

6183

42-5

AY

0617

77 A

Y61

6674

Isla

Ray

a A

zuer

o P

enin

sula

P

anam

a 7

infin23

64centN

80infin

160

2centW

Dir

ect

(obs

erve

d)F

MN

H 3

0648

2A

Y61

8327

AY

6166

73

Kan

eoh

e B

ay H

awai

i U

SA

[5 a

nim

als]

Pla

nkt

otro

phic

(B

ell

1993

)F

MN

H 2

8217

1-2

AY

0617

90A

Y06

1769

US

S M

ach

inis

t G

uam

[3

anim

als]

Not

obs

erve

dF

MN

H 2

8236

2A

Y06

1791

AY

0617

71Z

orri

tos

Per

u

3infin45

centS

80infin4

0centW

[20

anim

als]

Pla

nkt

otro

phic

(obs

erve

d)F

MN

H 2

8236

7A

Y06

1778

AY

0617

73

Los

Au

baz

Pai

ta P

eru

5infin1

0centS

81infin1

0centW

[20

an

imal

s]P

lan

ktot

roph

ic(o

bser

ved)

AN

SP

A19

746

FM

NH

28

2351

BM

2001

0454

AY

0617

85

AY

6183

29-3

2A

Y06

1772

B c

f te

guli

ciu

sC

alh

eta

Fu

nda

S

al I

slan

d C

ape

Ver

de

16infin4

0centN

22

infin03cent

W[1

an

imal

]

Dir

ect

(fro

mpr

otoc

onch

)F

MN

H 2

8235

9A

Y06

1776

AY

0617

75



B p

ritz

ker

i E

dwar

ds B

each

Syd

ney

Au

stra

lia

33

infin51cent

S 1

51infin1

3centE

[14

an

imal

s]T

YP

E L

OC

AL

ITY

Dir

ect

(obs

erve

d)F

MN

H 2

8230

2 A

NM

C40

0000

AY

0617

93 A

Y61

8348

AY

0617

67

B o

dit

es

Pla

ya O

ren

go n

ear

San

An

ton

ioO

este

Arg

enti

na

40infin

53centS

64

infin29cent

W [

gt25

an

imal

s]

Dir

ect

wit

h n

urs

eeg

gs (

obse

rved

)F

MN

H 2

8229

7A

NS

P A

1974

4B

M20

0104

56

AY

0617

82 A

Y06

1784

A

Y06

1794

AY

0617

62 A

Y06

1764

Woo

leyrsquo

s P

ool

Mu

izen

berg

Sou

thA

fric

a 3

4infin04

centS

18infin2

0centE

[15

anim

als]

TY

PE

LO

CA

LIT

Y

Dir

ect

wit

h n

urs

e eg

gs(o

bser

ved)

FM

NH

282

277

V94

47

T17

83 B

M20

0104

53A

Y06

1780

AY

0617

88ndash

Por

t E

liza

beth

Sou

th A

fric

a[2

an

imal

s]N

ot o

bser

ved

FM

NH

282

368

AY

0617

87A

Y06

1765

Goi

s B

each

San

tos

Bay

Satildeo

Pau

lo

Bra

zil

24infin

00centS

46infin

21centW

[5 a

nim

als]

Dir

ect

wit

h n

urs

eeg

gs (

from

prot

ocon

ch)

FM

NH

282

350

AY

0617

79 A

Y06

1781

AY

0617

63

B l

ate

bru

sE

l C

omit

aacuten n

ear

La

Paz

BC

SM

exic

o 2

4infin07

centN

110infin

24centW

[10

anim

als]

TY

PE

LO

CA

LIT

Y

Dir

ect

(obs

erve

d)F

MN

H 2

8219

3-4

AY

0617

89 A

Y61

8333

AY

0617

68

B u

rra

ca

Isla

Par

ida

Gu

lf o

f C

hir

iqu

iP

anam

a 8

infin54

58centN

82

infin18

671cent

W[

gt50

anim

als]

TY

PE

LO

CA

LIT

Y

Dir

ect

(obs

erve

d)A

NS

P 4

1217

8ndash9

FM

NH

306

483

AY

6183

19 A

Y61

8325

-6A

Y61

6667

-9

Isla

Ray

a A

zuer

o P

enin

sula

P

anam

a 7

infin23

64centN

80infin

160

2centW

Dir

ect

(obs

erve

d)F

MN

H 3

0648

4A

Y61

8321

ndash

Isla

Jac

aron

Par

que

Nat

ion

alC

oiba

P

anam

a 7

infin19

10centN

81

infin43

83centW

[3

anim

als]

Not

obs

erve

dK

LK

C I

CP

-03ndash

069

AY

6183

18 A

Y61

8320

A

Y61

8324

ndash

El

Sal

vado

r G

ulf

of

Fon

seca

13

infin26

4 N

89infin

480

4 W

[3 a

nim

als]

13infin1

723

N 8

9infin18

07

W [

1 an

imal

]N

ot o

bser

ved

AN

SP

412

180-

1A

Y61

8341

AY

6183

49A

Y61

6670

-2

Spe

cies

Loc

alit

yM

ode

of d

evel

opm

ent

Vou

cher

nos

G

enba

nk

nos

CO

IG

enba

nk

nos

16S

80 R COLLIN






RESULTS



DNA SEQUENCE DATA




MORPHOLOGY







82 R COLLIN


Tab

le 2

P

airw

ise

Kim

ura

2-p

aram

eter

gen

etic

dis

tan

ces

betw

een

in

divi

dual

s fr

om e

ach

loc

alit

y B

old

valu

es i

ndi

cate

in

tras

peci

fic

com

pari

son

s A

bbre

viat

ion

sA

rg A

rgen

tin

a B

ah B

aham

as

BP

Bay

of

Pan

ama

CT

Cap

e T

own

CV

Cap

e V

erde

E

S E

l S

alva

dor

GC

Gu

lf o

f C

hir

iqu

i

16S

CO

IC

VB

razi

lC

TA

rgJa

pan

Per

uB

PH

awai

iG

uam

Mex

ico

Flo

rida

Syd

ney

Bah

ES

GC

CV

ndash0

081

007

80

083

007

60

080

008

10

081

008

00

074

003

40

074

ndash0

068

007

5B

razi

l0

168

ndash0

062

000

60

067

005

10

054

005

40

054

006

90

073

007

0ndash

004

10

045

CT

016

60

012

ndash0

008

006

50

045

004

70

047

004

70

067

007

10

067

ndash0

038

004

3A

rg0

174

000

80

010

ndash0

069

005

40

056

005

60

056

007

20

075

007

2ndash

004

30

047

Japa

n0

211

015

80

154

015

6ndash

006

10

056

005

60

056

003

40

071

001

7ndash

005

90

068

Per

u0

185

012

60

126

012

60

174

ndash0

006

000

80

006

006

60

081

006

3ndash

005

20

054

BP

016

30

103

010

30

105

016

60

044

ndash0

002

000

00

061

008

10

059

ndash0

052

005

4H

awai

i0

166

010

30

103

010

50

166

004

60

002

ndash0

002

016

20

085

005

9ndash

005

20

056

Gu

am0

163

010

30

103

010

50

166

004

60

000

000

2ndash

016

20

085

005

9ndash

005

30

054

Mex

ico

018

60

144

014

00

138

010

60

164

016

20

061

006

1ndash

006

90

038

ndash0

073

007

7F

lori

da0

066

015

70

155

016

00

192

016

90

157

015

90

157

019

9ndash

006

9ndash

006

10

073

Syd

ney

017

40

133

012

80

131

009

40

152

014

00

140

014

00

122

017

4ndash

ndash0

056

007

2B

ah0

066

015

50

153

015

80

190

016

00

155

015

70

157

020

00

002

017

2ndash

ndashndash

ES

017

10

167

012

10

113

012

30

160

012

70

129

012

90

129

015

50

156

015

2ndash

000

8G

C0

161

011

90

111

012

10

163

012

10

123

012

30

123

016

70

152

015

60

151

000

7ndash







Peru

Panama

HawaiiGuam

84 R COLLIN









86 R COLLIN



DEVELOPMENT











A B

C D

DISCUSSION




88 R COLLIN


Tab

le 4

S

um

mar

y of

Bos

tryc

apu

lus

spec

ies

Dia

gnos

tic

feat

ure

s ar

e h

igh

ligh

ted

in b

old

text

A

bbre

viat

ion

s s

s s

pira

l sc

ulp

ture

B a

cule

atu

sB

gra

visp

inos

us

B c

alyp

trae

form

isB

teg

uli

ciu

sB

pri

tzke

riB

od

ites

B l

ateb

rus

B u

rrac

a

Au

thor

ity

(Gm

elin

179

1)(K

uro

da amp

Hab

e 1

950)

(Des

hay

es 1

830)

(Roc

heb

run

e18

83)

sp n

ov

sp n

ov

sp n

ov

sp n

ov

Fate

of

type

St

Pet

ersb

erg

un

know

nP

aris

Mu

seu

mP

aris

Mu

seu

mA

ust

rali

anM

use

um

Nat

alM

use

um

Fie

ld M

use

um

Fie

ld M

use

um

Typ

e lo

cali

tyM

iddl

eA

mer

ican

Isla

nds

Hir

ado

Is

Nag

asak

iP

ref

Japa

n

Per

u (

dubi

ous)

Sen

egal

Edw

ards

Ree

fS

ydn

ey

Au

stra

lia

Woo

leyrsquo

s P

ool

Cap

e T

own

S

A

La

Paz

BC

SM

exic

oG

ulf

of

Ch

iriq

ui

Pan

ama

Dev

elop

men

tdi

rect

dire

ctp

lan

kto

trop

hic

dire

ct (

from

prot

ocon

ch)

dire

ctd

irec

t w

ith

nu

rse

eggs

dire

ctdi

rect

Egg

siz

e (m

m)

380

(Hoa

glan

d 1

986)

200

(qu

esti

onab

le)

180

ndash53

0ndash56

019

848

837

0

(Am

io 1

963)

Hat

chin

g si

ze(m

m)

840

1000

ndash120

0 38

0ndash

ndashndash

ndash88

8(H

oagl

and

198

6)(I

shik

i 19

36)

Em

bryo

nic

oper

culu

mpr

esen

tndash

pres

ent

ndashab

sen

tpr

esen

tpr

esen

tpr

esen

t

Dis

tin

ct v

elu

mw

ith

foo

dgr

oove

med

ium

spo

tted

w

ith

foo

d gr

oove

ndashla

rge

pig

men

ted

ndashab

sen

tsm

all

un

pigm

ente

dsm

all

un

pigm

ente

dab

sen

t

Em

bryo

nic

sh

ell

scu

lptu

regr

anu

lar

ss

ss a

t h

atch

ing

(Am

io)

fin

e sp

ines

ove

ren

tire

lar

val

shel

l

ndashgr

anu

lar

sssm

ooth

wit

hir

regu

lar

grow

thli

nes

gran

ula

r ss

gran

ula

r ss

Pro

toco

nch

1 w

hor

l1

wh

orl

15

wh

orls

less

th

an 1

w

hor

ln

ot a

vail

able

125

wh

orls

less

th

an 1

w

hor

lle

ss t

han

1w

hor

lL

ocal

itie

sF

lori

da Y

uca

tan

B

aham

asJa

pan

Per

u

Pan

ama

Haw

aii

Gu

amW

est

Afr

ica

Cap

e V

erde

Is

Au

stra

lia

Sou

th A

fric

a

Pat

agon

ia

Bra

zil

La

Paz

Mex

ico

Pan

ama

El

Sal

vado

r










90 R COLLIN
























92 R COLLIN




































94 R COLLIN







































640





96 R COLLIN











A B C D























98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN















































SYSTEMATICS OF

BOSTRYCAPULUS

77



2005

144

75ndash101

Figure 1

Photographs of (A)



B odites

sp nov


=

10 mm

A

B

78

R COLLIN



2005

144

75ndash101

Tab

le 1

Su

mm

ary

of li

ve-c

olle

cted

mat

eria

l use

d fo

r ob

serv

atio

ns

of d

evel

opm

ent

and

anat

omy

and

for

DN

A s

equ

enci

ng

Abb

revi

atio

ns

BM

SM

Bai

ley-

Mat

thew

sS

hel

l M

use

um

K

LK

C K

L K

aise

r C

olle

ctio

n

Spe

cies

Loc

alit

yM

ode

of d

evel

opm

ent

Vou

cher

nos

G

enba

nk

nos

CO

IG

enba

nk

nos

16S

B a

cule

atu

s

M

ote

Mar

ine

Lab

orat

ory

Lid

o K

ey

Flo

rida

U

SA

27

infin

20

cent

N

82

infin

42

cent

W[

gt

30 a

nim

als]

Dir

ect

(obs

erve

d)A

NS

P A

1974

5F

MN

H 2

8236

5B

M20

0104

55

AY

0617

92 A

Y61

8322

-3A

Y06

1774

Har

bor

Bra

nch

Oce

anog

raph

icIn

stit

ute

F

lori

daU

SA

28

infin

29

cent

N 8

1

infin

20

cent

W [

3 an

imal

s]

Dir

ect

(obs

erve

d)F

MN

H 3

0648

1A

Y61

8317

ndash

Flo

rida

Key

s U

SA

24

infin

40

cent

50

cent

N

82

infin

16

cent

02

cent

W [

2 an

imal

s]D

irec

t (o

bser

ved)

FM

NH

282

284

AY

0617

77ndash

Aba

co B

aham

as 2

6

infin

42

cent

56

cent

N

77

infin

14

cent

33

cent

W [

5 an

imal

s]N

ot o

bser

ved

BM

SM

262

92B

MS

M 2

6293

B

MS

M 2

6294

BM

SM

262

95

AY

6183

46-7

ndash

B g

ravi

spin

osu

s

Ch

ijiw

a N

agas

aki

Japa

n[1

an

imal

]N

ot o

bser

ved

FM

NH

282

336

AY

0617

83A

Y06

1766

B c

alyp

trae

form

is

Pla

ya V

enad

o P

anam

a 8

infin

55

cent

N

79

infin

38

centW [

gt10

0 an

imal

s]P

lan

ktot

roph

ic(o

bser

ved)

FM

NH

282

273

AN

SP

A19

740

BM

2001

0452

AY

0617

86 A

Y61

8328

AY

6183

34-4

0

AY

6183

42-5

AY

0617

77 A

Y61

6674

Isla

Ray

a A

zuer

o P

enin

sula

P

anam

a 7

infin23

64centN

80infin

160

2centW

Dir

ect

(obs

erve

d)F

MN

H 3

0648

2A

Y61

8327

AY

6166

73

Kan

eoh

e B

ay H

awai

i U

SA

[5 a

nim

als]

Pla

nkt

otro

phic

(B

ell

1993

)F

MN

H 2

8217

1-2

AY

0617

90A

Y06

1769

US

S M

ach

inis

t G

uam

[3

anim

als]

Not

obs

erve

dF

MN

H 2

8236

2A

Y06

1791

AY

0617

71Z

orri

tos

Per

u

3infin45

centS

80infin4

0centW

[20

anim

als]

Pla

nkt

otro

phic

(obs

erve

d)F

MN

H 2

8236

7A

Y06

1778

AY

0617

73

Los

Au

baz

Pai

ta P

eru

5infin1

0centS

81infin1

0centW

[20

an

imal

s]P

lan

ktot

roph

ic(o

bser

ved)

AN

SP

A19

746

FM

NH

28

2351

BM

2001

0454

AY

0617

85

AY

6183

29-3

2A

Y06

1772

B c

f te

guli

ciu

sC

alh

eta

Fu

nda

S

al I

slan

d C

ape

Ver

de

16infin4

0centN

22

infin03cent

W[1

an

imal

]

Dir

ect

(fro

mpr

otoc

onch

)F

MN

H 2

8235

9A

Y06

1776

AY

0617

75



B p

ritz

ker

i E

dwar

ds B

each

Syd

ney

Au

stra

lia

33

infin51cent

S 1

51infin1

3centE

[14

an

imal

s]T

YP

E L

OC

AL

ITY

Dir

ect

(obs

erve

d)F

MN

H 2

8230

2 A

NM

C40

0000

AY

0617

93 A

Y61

8348

AY

0617

67

B o

dit

es

Pla

ya O

ren

go n

ear

San

An

ton

ioO

este

Arg

enti

na

40infin

53centS

64

infin29cent

W [

gt25

an

imal

s]

Dir

ect

wit

h n

urs

eeg

gs (

obse

rved

)F

MN

H 2

8229

7A

NS

P A

1974

4B

M20

0104

56

AY

0617

82 A

Y06

1784

A

Y06

1794

AY

0617

62 A

Y06

1764

Woo

leyrsquo

s P

ool

Mu

izen

berg

Sou

thA

fric

a 3

4infin04

centS

18infin2

0centE

[15

anim

als]

TY

PE

LO

CA

LIT

Y

Dir

ect

wit

h n

urs

e eg

gs(o

bser

ved)

FM

NH

282

277

V94

47

T17

83 B

M20

0104

53A

Y06

1780

AY

0617

88ndash

Por

t E

liza

beth

Sou

th A

fric

a[2

an

imal

s]N

ot o

bser

ved

FM

NH

282

368

AY

0617

87A

Y06

1765

Goi

s B

each

San

tos

Bay

Satildeo

Pau

lo

Bra

zil

24infin

00centS

46infin

21centW

[5 a

nim

als]

Dir

ect

wit

h n

urs

eeg

gs (

from

prot

ocon

ch)

FM

NH

282

350

AY

0617

79 A

Y06

1781

AY

0617

63

B l

ate

bru

sE

l C

omit

aacuten n

ear

La

Paz

BC

SM

exic

o 2

4infin07

centN

110infin

24centW

[10

anim

als]

TY

PE

LO

CA

LIT

Y

Dir

ect

(obs

erve

d)F

MN

H 2

8219

3-4

AY

0617

89 A

Y61

8333

AY

0617

68

B u

rra

ca

Isla

Par

ida

Gu

lf o

f C

hir

iqu

iP

anam

a 8

infin54

58centN

82

infin18

671cent

W[

gt50

anim

als]

TY

PE

LO

CA

LIT

Y

Dir

ect

(obs

erve

d)A

NS

P 4

1217

8ndash9

FM

NH

306

483

AY

6183

19 A

Y61

8325

-6A

Y61

6667

-9

Isla

Ray

a A

zuer

o P

enin

sula

P

anam

a 7

infin23

64centN

80infin

160

2centW

Dir

ect

(obs

erve

d)F

MN

H 3

0648

4A

Y61

8321

ndash

Isla

Jac

aron

Par

que

Nat

ion

alC

oiba

P

anam

a 7

infin19

10centN

81

infin43

83centW

[3

anim

als]

Not

obs

erve

dK

LK

C I

CP

-03ndash

069

AY

6183

18 A

Y61

8320

A

Y61

8324

ndash

El

Sal

vado

r G

ulf

of

Fon

seca

13

infin26

4 N

89infin

480

4 W

[3 a

nim

als]

13infin1

723

N 8

9infin18

07

W [

1 an

imal

]N

ot o

bser

ved

AN

SP

412

180-

1A

Y61

8341

AY

6183

49A

Y61

6670

-2

Spe

cies

Loc

alit

yM

ode

of d

evel

opm

ent

Vou

cher

nos

G

enba

nk

nos

CO

IG

enba

nk

nos

16S

80 R COLLIN






RESULTS



DNA SEQUENCE DATA




MORPHOLOGY







82 R COLLIN


Tab

le 2

P

airw

ise

Kim

ura

2-p

aram

eter

gen

etic

dis

tan

ces

betw

een

in

divi

dual

s fr

om e

ach

loc

alit

y B

old

valu

es i

ndi

cate

in

tras

peci

fic

com

pari

son

s A

bbre

viat

ion

sA

rg A

rgen

tin

a B

ah B

aham

as

BP

Bay

of

Pan

ama

CT

Cap

e T

own

CV

Cap

e V

erde

E

S E

l S

alva

dor

GC

Gu

lf o

f C

hir

iqu

i

16S

CO

IC

VB

razi

lC

TA

rgJa

pan

Per

uB

PH

awai

iG

uam

Mex

ico

Flo

rida

Syd

ney

Bah

ES

GC

CV

ndash0

081

007

80

083

007

60

080

008

10

081

008

00

074

003

40

074

ndash0

068

007

5B

razi

l0

168

ndash0

062

000

60

067

005

10

054

005

40

054

006

90

073

007

0ndash

004

10

045

CT

016

60

012

ndash0

008

006

50

045

004

70

047

004

70

067

007

10

067

ndash0

038

004

3A

rg0

174

000

80

010

ndash0

069

005

40

056

005

60

056

007

20

075

007

2ndash

004

30

047

Japa

n0

211

015

80

154

015

6ndash

006

10

056

005

60

056

003

40

071

001

7ndash

005

90

068

Per

u0

185

012

60

126

012

60

174

ndash0

006

000

80

006

006

60

081

006

3ndash

005

20

054

BP

016

30

103

010

30

105

016

60

044

ndash0

002

000

00

061

008

10

059

ndash0

052

005

4H

awai

i0

166

010

30

103

010

50

166

004

60

002

ndash0

002

016

20

085

005

9ndash

005

20

056

Gu

am0

163

010

30

103

010

50

166

004

60

000

000

2ndash

016

20

085

005

9ndash

005

30

054

Mex

ico

018

60

144

014

00

138

010

60

164

016

20

061

006

1ndash

006

90

038

ndash0

073

007

7F

lori

da0

066

015

70

155

016

00

192

016

90

157

015

90

157

019

9ndash

006

9ndash

006

10

073

Syd

ney

017

40

133

012

80

131

009

40

152

014

00

140

014

00

122

017

4ndash

ndash0

056

007

2B

ah0

066

015

50

153

015

80

190

016

00

155

015

70

157

020

00

002

017

2ndash

ndashndash

ES

017

10

167

012

10

113

012

30

160

012

70

129

012

90

129

015

50

156

015

2ndash

000

8G

C0

161

011

90

111

012

10

163

012

10

123

012

30

123

016

70

152

015

60

151

000

7ndash







Peru

Panama

HawaiiGuam

84 R COLLIN









86 R COLLIN



DEVELOPMENT











A B

C D

DISCUSSION




88 R COLLIN


Tab

le 4

S

um

mar

y of

Bos

tryc

apu

lus

spec

ies

Dia

gnos

tic

feat

ure

s ar

e h

igh

ligh

ted

in b

old

text

A

bbre

viat

ion

s s

s s

pira

l sc

ulp

ture

B a

cule

atu

sB

gra

visp

inos

us

B c

alyp

trae

form

isB

teg

uli

ciu

sB

pri

tzke

riB

od

ites

B l

ateb

rus

B u

rrac

a

Au

thor

ity

(Gm

elin

179

1)(K

uro

da amp

Hab

e 1

950)

(Des

hay

es 1

830)

(Roc

heb

run

e18

83)

sp n

ov

sp n

ov

sp n

ov

sp n

ov

Fate

of

type

St

Pet

ersb

erg

un

know

nP

aris

Mu

seu

mP

aris

Mu

seu

mA

ust

rali

anM

use

um

Nat

alM

use

um

Fie

ld M

use

um

Fie

ld M

use

um

Typ

e lo

cali

tyM

iddl

eA

mer

ican

Isla

nds

Hir

ado

Is

Nag

asak

iP

ref

Japa

n

Per

u (

dubi

ous)

Sen

egal

Edw

ards

Ree

fS

ydn

ey

Au

stra

lia

Woo

leyrsquo

s P

ool

Cap

e T

own

S

A

La

Paz

BC

SM

exic

oG

ulf

of

Ch

iriq

ui

Pan

ama

Dev

elop

men

tdi

rect

dire

ctp

lan

kto

trop

hic

dire

ct (

from

prot

ocon

ch)

dire

ctd

irec

t w

ith

nu

rse

eggs

dire

ctdi

rect

Egg

siz

e (m

m)

380

(Hoa

glan

d 1

986)

200

(qu

esti

onab

le)

180

ndash53

0ndash56

019

848

837

0

(Am

io 1

963)

Hat

chin

g si

ze(m

m)

840

1000

ndash120

0 38

0ndash

ndashndash

ndash88

8(H

oagl

and

198

6)(I

shik

i 19

36)

Em

bryo

nic

oper

culu

mpr

esen

tndash

pres

ent

ndashab

sen

tpr

esen

tpr

esen

tpr

esen

t

Dis

tin

ct v

elu

mw

ith

foo

dgr

oove

med

ium

spo

tted

w

ith

foo

d gr

oove

ndashla

rge

pig

men

ted

ndashab

sen

tsm

all

un

pigm

ente

dsm

all

un

pigm

ente

dab

sen

t

Em

bryo

nic

sh

ell

scu

lptu

regr

anu

lar

ss

ss a

t h

atch

ing

(Am

io)

fin

e sp

ines

ove

ren

tire

lar

val

shel

l

ndashgr

anu

lar

sssm

ooth

wit

hir

regu

lar

grow

thli

nes

gran

ula

r ss

gran

ula

r ss

Pro

toco

nch

1 w

hor

l1

wh

orl

15

wh

orls

less

th

an 1

w

hor

ln

ot a

vail

able

125

wh

orls

less

th

an 1

w

hor

lle

ss t

han

1w

hor

lL

ocal

itie

sF

lori

da Y

uca

tan

B

aham

asJa

pan

Per

u

Pan

ama

Haw

aii

Gu

amW

est

Afr

ica

Cap

e V

erde

Is

Au

stra

lia

Sou

th A

fric

a

Pat

agon

ia

Bra

zil

La

Paz

Mex

ico

Pan

ama

El

Sal

vado

r










90 R COLLIN
























92 R COLLIN




































94 R COLLIN







































640





96 R COLLIN











A B C D























98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN















































78

R COLLIN



2005

144

75ndash101

Tab

le 1

Su

mm

ary

of li

ve-c

olle

cted

mat

eria

l use

d fo

r ob

serv

atio

ns

of d

evel

opm

ent

and

anat

omy

and

for

DN

A s

equ

enci

ng

Abb

revi

atio

ns

BM

SM

Bai

ley-

Mat

thew

sS

hel

l M

use

um

K

LK

C K

L K

aise

r C

olle

ctio

n

Spe

cies

Loc

alit

yM

ode

of d

evel

opm

ent

Vou

cher

nos

G

enba

nk

nos

CO

IG

enba

nk

nos

16S

B a

cule

atu

s

M

ote

Mar

ine

Lab

orat

ory

Lid

o K

ey

Flo

rida

U

SA

27

infin

20

cent

N

82

infin

42

cent

W[

gt

30 a

nim

als]

Dir

ect

(obs

erve

d)A

NS

P A

1974

5F

MN

H 2

8236

5B

M20

0104

55

AY

0617

92 A

Y61

8322

-3A

Y06

1774

Har

bor

Bra

nch

Oce

anog

raph

icIn

stit

ute

F

lori

daU

SA

28

infin

29

cent

N 8

1

infin

20

cent

W [

3 an

imal

s]

Dir

ect

(obs

erve

d)F

MN

H 3

0648

1A

Y61

8317

ndash

Flo

rida

Key

s U

SA

24

infin

40

cent

50

cent

N

82

infin

16

cent

02

cent

W [

2 an

imal

s]D

irec

t (o

bser

ved)

FM

NH

282

284

AY

0617

77ndash

Aba

co B

aham

as 2

6

infin

42

cent

56

cent

N

77

infin

14

cent

33

cent

W [

5 an

imal

s]N

ot o

bser

ved

BM

SM

262

92B

MS

M 2

6293

B

MS

M 2

6294

BM

SM

262

95

AY

6183

46-7

ndash

B g

ravi

spin

osu

s

Ch

ijiw

a N

agas

aki

Japa

n[1

an

imal

]N

ot o

bser

ved

FM

NH

282

336

AY

0617

83A

Y06

1766

B c

alyp

trae

form

is

Pla

ya V

enad

o P

anam

a 8

infin

55

cent

N

79

infin

38

centW [

gt10

0 an

imal

s]P

lan

ktot

roph

ic(o

bser

ved)

FM

NH

282

273

AN

SP

A19

740

BM

2001

0452

AY

0617

86 A

Y61

8328

AY

6183

34-4

0

AY

6183

42-5

AY

0617

77 A

Y61

6674

Isla

Ray

a A

zuer

o P

enin

sula

P

anam

a 7

infin23

64centN

80infin

160

2centW

Dir

ect

(obs

erve

d)F

MN

H 3

0648

2A

Y61

8327

AY

6166

73

Kan

eoh

e B

ay H

awai

i U

SA

[5 a

nim

als]

Pla

nkt

otro

phic

(B

ell

1993

)F

MN

H 2

8217

1-2

AY

0617

90A

Y06

1769

US

S M

ach

inis

t G

uam

[3

anim

als]

Not

obs

erve

dF

MN

H 2

8236

2A

Y06

1791

AY

0617

71Z

orri

tos

Per

u

3infin45

centS

80infin4

0centW

[20

anim

als]

Pla

nkt

otro

phic

(obs

erve

d)F

MN

H 2

8236

7A

Y06

1778

AY

0617

73

Los

Au

baz

Pai

ta P

eru

5infin1

0centS

81infin1

0centW

[20

an

imal

s]P

lan

ktot

roph

ic(o

bser

ved)

AN

SP

A19

746

FM

NH

28

2351

BM

2001

0454

AY

0617

85

AY

6183

29-3

2A

Y06

1772

B c

f te

guli

ciu

sC

alh

eta

Fu

nda

S

al I

slan

d C

ape

Ver

de

16infin4

0centN

22

infin03cent

W[1

an

imal

]

Dir

ect

(fro

mpr

otoc

onch

)F

MN

H 2

8235

9A

Y06

1776

AY

0617

75



B p

ritz

ker

i E

dwar

ds B

each

Syd

ney

Au

stra

lia

33

infin51cent

S 1

51infin1

3centE

[14

an

imal

s]T

YP

E L

OC

AL

ITY

Dir

ect

(obs

erve

d)F

MN

H 2

8230

2 A

NM

C40

0000

AY

0617

93 A

Y61

8348

AY

0617

67

B o

dit

es

Pla

ya O

ren

go n

ear

San

An

ton

ioO

este

Arg

enti

na

40infin

53centS

64

infin29cent

W [

gt25

an

imal

s]

Dir

ect

wit

h n

urs

eeg

gs (

obse

rved

)F

MN

H 2

8229

7A

NS

P A

1974

4B

M20

0104

56

AY

0617

82 A

Y06

1784

A

Y06

1794

AY

0617

62 A

Y06

1764

Woo

leyrsquo

s P

ool

Mu

izen

berg

Sou

thA

fric

a 3

4infin04

centS

18infin2

0centE

[15

anim

als]

TY

PE

LO

CA

LIT

Y

Dir

ect

wit

h n

urs

e eg

gs(o

bser

ved)

FM

NH

282

277

V94

47

T17

83 B

M20

0104

53A

Y06

1780

AY

0617

88ndash

Por

t E

liza

beth

Sou

th A

fric

a[2

an

imal

s]N

ot o

bser

ved

FM

NH

282

368

AY

0617

87A

Y06

1765

Goi

s B

each

San

tos

Bay

Satildeo

Pau

lo

Bra

zil

24infin

00centS

46infin

21centW

[5 a

nim

als]

Dir

ect

wit

h n

urs

eeg

gs (

from

prot

ocon

ch)

FM

NH

282

350

AY

0617

79 A

Y06

1781

AY

0617

63

B l

ate

bru

sE

l C

omit

aacuten n

ear

La

Paz

BC

SM

exic

o 2

4infin07

centN

110infin

24centW

[10

anim

als]

TY

PE

LO

CA

LIT

Y

Dir

ect

(obs

erve

d)F

MN

H 2

8219

3-4

AY

0617

89 A

Y61

8333

AY

0617

68

B u

rra

ca

Isla

Par

ida

Gu

lf o

f C

hir

iqu

iP

anam

a 8

infin54

58centN

82

infin18

671cent

W[

gt50

anim

als]

TY

PE

LO

CA

LIT

Y

Dir

ect

(obs

erve

d)A

NS

P 4

1217

8ndash9

FM

NH

306

483

AY

6183

19 A

Y61

8325

-6A

Y61

6667

-9

Isla

Ray

a A

zuer

o P

enin

sula

P

anam

a 7

infin23

64centN

80infin

160

2centW

Dir

ect

(obs

erve

d)F

MN

H 3

0648

4A

Y61

8321

ndash

Isla

Jac

aron

Par

que

Nat

ion

alC

oiba

P

anam

a 7

infin19

10centN

81

infin43

83centW

[3

anim

als]

Not

obs

erve

dK

LK

C I

CP

-03ndash

069

AY

6183

18 A

Y61

8320

A

Y61

8324

ndash

El

Sal

vado

r G

ulf

of

Fon

seca

13

infin26

4 N

89infin

480

4 W

[3 a

nim

als]

13infin1

723

N 8

9infin18

07

W [

1 an

imal

]N

ot o

bser

ved

AN

SP

412

180-

1A

Y61

8341

AY

6183

49A

Y61

6670

-2

Spe

cies

Loc

alit

yM

ode

of d

evel

opm

ent

Vou

cher

nos

G

enba

nk

nos

CO

IG

enba

nk

nos

16S

80 R COLLIN






RESULTS



DNA SEQUENCE DATA




MORPHOLOGY







82 R COLLIN


Tab

le 2

P

airw

ise

Kim

ura

2-p

aram

eter

gen

etic

dis

tan

ces

betw

een

in

divi

dual

s fr

om e

ach

loc

alit

y B

old

valu

es i

ndi

cate

in

tras

peci

fic

com

pari

son

s A

bbre

viat

ion

sA

rg A

rgen

tin

a B

ah B

aham

as

BP

Bay

of

Pan

ama

CT

Cap

e T

own

CV

Cap

e V

erde

E

S E

l S

alva

dor

GC

Gu

lf o

f C

hir

iqu

i

16S

CO

IC

VB

razi

lC

TA

rgJa

pan

Per

uB

PH

awai

iG

uam

Mex

ico

Flo

rida

Syd

ney

Bah

ES

GC

CV

ndash0

081

007

80

083

007

60

080

008

10

081

008

00

074

003

40

074

ndash0

068

007

5B

razi

l0

168

ndash0

062

000

60

067

005

10

054

005

40

054

006

90

073

007

0ndash

004

10

045

CT

016

60

012

ndash0

008

006

50

045

004

70

047

004

70

067

007

10

067

ndash0

038

004

3A

rg0

174

000

80

010

ndash0

069

005

40

056

005

60

056

007

20

075

007

2ndash

004

30

047

Japa

n0

211

015

80

154

015

6ndash

006

10

056

005

60

056

003

40

071

001

7ndash

005

90

068

Per

u0

185

012

60

126

012

60

174

ndash0

006

000

80

006

006

60

081

006

3ndash

005

20

054

BP

016

30

103

010

30

105

016

60

044

ndash0

002

000

00

061

008

10

059

ndash0

052

005

4H

awai

i0

166

010

30

103

010

50

166

004

60

002

ndash0

002

016

20

085

005

9ndash

005

20

056

Gu

am0

163

010

30

103

010

50

166

004

60

000

000

2ndash

016

20

085

005

9ndash

005

30

054

Mex

ico

018

60

144

014

00

138

010

60

164

016

20

061

006

1ndash

006

90

038

ndash0

073

007

7F

lori

da0

066

015

70

155

016

00

192

016

90

157

015

90

157

019

9ndash

006

9ndash

006

10

073

Syd

ney

017

40

133

012

80

131

009

40

152

014

00

140

014

00

122

017

4ndash

ndash0

056

007

2B

ah0

066

015

50

153

015

80

190

016

00

155

015

70

157

020

00

002

017

2ndash

ndashndash

ES

017

10

167

012

10

113

012

30

160

012

70

129

012

90

129

015

50

156

015

2ndash

000

8G

C0

161

011

90

111

012

10

163

012

10

123

012

30

123

016

70

152

015

60

151

000

7ndash







Peru

Panama

HawaiiGuam

84 R COLLIN









86 R COLLIN



DEVELOPMENT











A B

C D

DISCUSSION




88 R COLLIN


Tab

le 4

S

um

mar

y of

Bos

tryc

apu

lus

spec

ies

Dia

gnos

tic

feat

ure

s ar

e h

igh

ligh

ted

in b

old

text

A

bbre

viat

ion

s s

s s

pira

l sc

ulp

ture

B a

cule

atu

sB

gra

visp

inos

us

B c

alyp

trae

form

isB

teg

uli

ciu

sB

pri

tzke

riB

od

ites

B l

ateb

rus

B u

rrac

a

Au

thor

ity

(Gm

elin

179

1)(K

uro

da amp

Hab

e 1

950)

(Des

hay

es 1

830)

(Roc

heb

run

e18

83)

sp n

ov

sp n

ov

sp n

ov

sp n

ov

Fate

of

type

St

Pet

ersb

erg

un

know

nP

aris

Mu

seu

mP

aris

Mu

seu

mA

ust

rali

anM

use

um

Nat

alM

use

um

Fie

ld M

use

um

Fie

ld M

use

um

Typ

e lo

cali

tyM

iddl

eA

mer

ican

Isla

nds

Hir

ado

Is

Nag

asak

iP

ref

Japa

n

Per

u (

dubi

ous)

Sen

egal

Edw

ards

Ree

fS

ydn

ey

Au

stra

lia

Woo

leyrsquo

s P

ool

Cap

e T

own

S

A

La

Paz

BC

SM

exic

oG

ulf

of

Ch

iriq

ui

Pan

ama

Dev

elop

men

tdi

rect

dire

ctp

lan

kto

trop

hic

dire

ct (

from

prot

ocon

ch)

dire

ctd

irec

t w

ith

nu

rse

eggs

dire

ctdi

rect

Egg

siz

e (m

m)

380

(Hoa

glan

d 1

986)

200

(qu

esti

onab

le)

180

ndash53

0ndash56

019

848

837

0

(Am

io 1

963)

Hat

chin

g si

ze(m

m)

840

1000

ndash120

0 38

0ndash

ndashndash

ndash88

8(H

oagl

and

198

6)(I

shik

i 19

36)

Em

bryo

nic

oper

culu

mpr

esen

tndash

pres

ent

ndashab

sen

tpr

esen

tpr

esen

tpr

esen

t

Dis

tin

ct v

elu

mw

ith

foo

dgr

oove

med

ium

spo

tted

w

ith

foo

d gr

oove

ndashla

rge

pig

men

ted

ndashab

sen

tsm

all

un

pigm

ente

dsm

all

un

pigm

ente

dab

sen

t

Em

bryo

nic

sh

ell

scu

lptu

regr

anu

lar

ss

ss a

t h

atch

ing

(Am

io)

fin

e sp

ines

ove

ren

tire

lar

val

shel

l

ndashgr

anu

lar

sssm

ooth

wit

hir

regu

lar

grow

thli

nes

gran

ula

r ss

gran

ula

r ss

Pro

toco

nch

1 w

hor

l1

wh

orl

15

wh

orls

less

th

an 1

w

hor

ln

ot a

vail

able

125

wh

orls

less

th

an 1

w

hor

lle

ss t

han

1w

hor

lL

ocal

itie

sF

lori

da Y

uca

tan

B

aham

asJa

pan

Per

u

Pan

ama

Haw

aii

Gu

amW

est

Afr

ica

Cap

e V

erde

Is

Au

stra

lia

Sou

th A

fric

a

Pat

agon

ia

Bra

zil

La

Paz

Mex

ico

Pan

ama

El

Sal

vado

r










90 R COLLIN
























92 R COLLIN




































94 R COLLIN







































640





96 R COLLIN











A B C D























98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN

















































B p

ritz

ker

i E

dwar

ds B

each

Syd

ney

Au

stra

lia

33

infin51cent

S 1

51infin1

3centE

[14

an

imal

s]T

YP

E L

OC

AL

ITY

Dir

ect

(obs

erve

d)F

MN

H 2

8230

2 A

NM

C40

0000

AY

0617

93 A

Y61

8348

AY

0617

67

B o

dit

es

Pla

ya O

ren

go n

ear

San

An

ton

ioO

este

Arg

enti

na

40infin

53centS

64

infin29cent

W [

gt25

an

imal

s]

Dir

ect

wit

h n

urs

eeg

gs (

obse

rved

)F

MN

H 2

8229

7A

NS

P A

1974

4B

M20

0104

56

AY

0617

82 A

Y06

1784

A

Y06

1794

AY

0617

62 A

Y06

1764

Woo

leyrsquo

s P

ool

Mu

izen

berg

Sou

thA

fric

a 3

4infin04

centS

18infin2

0centE

[15

anim

als]

TY

PE

LO

CA

LIT

Y

Dir

ect

wit

h n

urs

e eg

gs(o

bser

ved)

FM

NH

282

277

V94

47

T17

83 B

M20

0104

53A

Y06

1780

AY

0617

88ndash

Por

t E

liza

beth

Sou

th A

fric

a[2

an

imal

s]N

ot o

bser

ved

FM

NH

282

368

AY

0617

87A

Y06

1765

Goi

s B

each

San

tos

Bay

Satildeo

Pau

lo

Bra

zil

24infin

00centS

46infin

21centW

[5 a

nim

als]

Dir

ect

wit

h n

urs

eeg

gs (

from

prot

ocon

ch)

FM

NH

282

350

AY

0617

79 A

Y06

1781

AY

0617

63

B l

ate

bru

sE

l C

omit

aacuten n

ear

La

Paz

BC

SM

exic

o 2

4infin07

centN

110infin

24centW

[10

anim

als]

TY

PE

LO

CA

LIT

Y

Dir

ect

(obs

erve

d)F

MN

H 2

8219

3-4

AY

0617

89 A

Y61

8333

AY

0617

68

B u

rra

ca

Isla

Par

ida

Gu

lf o

f C

hir

iqu

iP

anam

a 8

infin54

58centN

82

infin18

671cent

W[

gt50

anim

als]

TY

PE

LO

CA

LIT

Y

Dir

ect

(obs

erve

d)A

NS

P 4

1217

8ndash9

FM

NH

306

483

AY

6183

19 A

Y61

8325

-6A

Y61

6667

-9

Isla

Ray

a A

zuer

o P

enin

sula

P

anam

a 7

infin23

64centN

80infin

160

2centW

Dir

ect

(obs

erve

d)F

MN

H 3

0648

4A

Y61

8321

ndash

Isla

Jac

aron

Par

que

Nat

ion

alC

oiba

P

anam

a 7

infin19

10centN

81

infin43

83centW

[3

anim

als]

Not

obs

erve

dK

LK

C I

CP

-03ndash

069

AY

6183

18 A

Y61

8320

A

Y61

8324

ndash

El

Sal

vado

r G

ulf

of

Fon

seca

13

infin26

4 N

89infin

480

4 W

[3 a

nim

als]

13infin1

723

N 8

9infin18

07

W [

1 an

imal

]N

ot o

bser

ved

AN

SP

412

180-

1A

Y61

8341

AY

6183

49A

Y61

6670

-2

Spe

cies

Loc

alit

yM

ode

of d

evel

opm

ent

Vou

cher

nos

G

enba

nk

nos

CO

IG

enba

nk

nos

16S

80 R COLLIN






RESULTS



DNA SEQUENCE DATA




MORPHOLOGY







82 R COLLIN


Tab

le 2

P

airw

ise

Kim

ura

2-p

aram

eter

gen

etic

dis

tan

ces

betw

een

in

divi

dual

s fr

om e

ach

loc

alit

y B

old

valu

es i

ndi

cate

in

tras

peci

fic

com

pari

son

s A

bbre

viat

ion

sA

rg A

rgen

tin

a B

ah B

aham

as

BP

Bay

of

Pan

ama

CT

Cap

e T

own

CV

Cap

e V

erde

E

S E

l S

alva

dor

GC

Gu

lf o

f C

hir

iqu

i

16S

CO

IC

VB

razi

lC

TA

rgJa

pan

Per

uB

PH

awai

iG

uam

Mex

ico

Flo

rida

Syd

ney

Bah

ES

GC

CV

ndash0

081

007

80

083

007

60

080

008

10

081

008

00

074

003

40

074

ndash0

068

007

5B

razi

l0

168

ndash0

062

000

60

067

005

10

054

005

40

054

006

90

073

007

0ndash

004

10

045

CT

016

60

012

ndash0

008

006

50

045

004

70

047

004

70

067

007

10

067

ndash0

038

004

3A

rg0

174

000

80

010

ndash0

069

005

40

056

005

60

056

007

20

075

007

2ndash

004

30

047

Japa

n0

211

015

80

154

015

6ndash

006

10

056

005

60

056

003

40

071

001

7ndash

005

90

068

Per

u0

185

012

60

126

012

60

174

ndash0

006

000

80

006

006

60

081

006

3ndash

005

20

054

BP

016

30

103

010

30

105

016

60

044

ndash0

002

000

00

061

008

10

059

ndash0

052

005

4H

awai

i0

166

010

30

103

010

50

166

004

60

002

ndash0

002

016

20

085

005

9ndash

005

20

056

Gu

am0

163

010

30

103

010

50

166

004

60

000

000

2ndash

016

20

085

005

9ndash

005

30

054

Mex

ico

018

60

144

014

00

138

010

60

164

016

20

061

006

1ndash

006

90

038

ndash0

073

007

7F

lori

da0

066

015

70

155

016

00

192

016

90

157

015

90

157

019

9ndash

006

9ndash

006

10

073

Syd

ney

017

40

133

012

80

131

009

40

152

014

00

140

014

00

122

017

4ndash

ndash0

056

007

2B

ah0

066

015

50

153

015

80

190

016

00

155

015

70

157

020

00

002

017

2ndash

ndashndash

ES

017

10

167

012

10

113

012

30

160

012

70

129

012

90

129

015

50

156

015

2ndash

000

8G

C0

161

011

90

111

012

10

163

012

10

123

012

30

123

016

70

152

015

60

151

000

7ndash







Peru

Panama

HawaiiGuam

84 R COLLIN









86 R COLLIN



DEVELOPMENT











A B

C D

DISCUSSION




88 R COLLIN


Tab

le 4

S

um

mar

y of

Bos

tryc

apu

lus

spec

ies

Dia

gnos

tic

feat

ure

s ar

e h

igh

ligh

ted

in b

old

text

A

bbre

viat

ion

s s

s s

pira

l sc

ulp

ture

B a

cule

atu

sB

gra

visp

inos

us

B c

alyp

trae

form

isB

teg

uli

ciu

sB

pri

tzke

riB

od

ites

B l

ateb

rus

B u

rrac

a

Au

thor

ity

(Gm

elin

179

1)(K

uro

da amp

Hab

e 1

950)

(Des

hay

es 1

830)

(Roc

heb

run

e18

83)

sp n

ov

sp n

ov

sp n

ov

sp n

ov

Fate

of

type

St

Pet

ersb

erg

un

know

nP

aris

Mu

seu

mP

aris

Mu

seu

mA

ust

rali

anM

use

um

Nat

alM

use

um

Fie

ld M

use

um

Fie

ld M

use

um

Typ

e lo

cali

tyM

iddl

eA

mer

ican

Isla

nds

Hir

ado

Is

Nag

asak

iP

ref

Japa

n

Per

u (

dubi

ous)

Sen

egal

Edw

ards

Ree

fS

ydn

ey

Au

stra

lia

Woo

leyrsquo

s P

ool

Cap

e T

own

S

A

La

Paz

BC

SM

exic

oG

ulf

of

Ch

iriq

ui

Pan

ama

Dev

elop

men

tdi

rect

dire

ctp

lan

kto

trop

hic

dire

ct (

from

prot

ocon

ch)

dire

ctd

irec

t w

ith

nu

rse

eggs

dire

ctdi

rect

Egg

siz

e (m

m)

380

(Hoa

glan

d 1

986)

200

(qu

esti

onab

le)

180

ndash53

0ndash56

019

848

837

0

(Am

io 1

963)

Hat

chin

g si

ze(m

m)

840

1000

ndash120

0 38

0ndash

ndashndash

ndash88

8(H

oagl

and

198

6)(I

shik

i 19

36)

Em

bryo

nic

oper

culu

mpr

esen

tndash

pres

ent

ndashab

sen

tpr

esen

tpr

esen

tpr

esen

t

Dis

tin

ct v

elu

mw

ith

foo

dgr

oove

med

ium

spo

tted

w

ith

foo

d gr

oove

ndashla

rge

pig

men

ted

ndashab

sen

tsm

all

un

pigm

ente

dsm

all

un

pigm

ente

dab

sen

t

Em

bryo

nic

sh

ell

scu

lptu

regr

anu

lar

ss

ss a

t h

atch

ing

(Am

io)

fin

e sp

ines

ove

ren

tire

lar

val

shel

l

ndashgr

anu

lar

sssm

ooth

wit

hir

regu

lar

grow

thli

nes

gran

ula

r ss

gran

ula

r ss

Pro

toco

nch

1 w

hor

l1

wh

orl

15

wh

orls

less

th

an 1

w

hor

ln

ot a

vail

able

125

wh

orls

less

th

an 1

w

hor

lle

ss t

han

1w

hor

lL

ocal

itie

sF

lori

da Y

uca

tan

B

aham

asJa

pan

Per

u

Pan

ama

Haw

aii

Gu

amW

est

Afr

ica

Cap

e V

erde

Is

Au

stra

lia

Sou

th A

fric

a

Pat

agon

ia

Bra

zil

La

Paz

Mex

ico

Pan

ama

El

Sal

vado

r










90 R COLLIN
























92 R COLLIN




































94 R COLLIN







































640





96 R COLLIN











A B C D























98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN















































80 R COLLIN






RESULTS



DNA SEQUENCE DATA




MORPHOLOGY







82 R COLLIN


Tab

le 2

P

airw

ise

Kim

ura

2-p

aram

eter

gen

etic

dis

tan

ces

betw

een

in

divi

dual

s fr

om e

ach

loc

alit

y B

old

valu

es i

ndi

cate

in

tras

peci

fic

com

pari

son

s A

bbre

viat

ion

sA

rg A

rgen

tin

a B

ah B

aham

as

BP

Bay

of

Pan

ama

CT

Cap

e T

own

CV

Cap

e V

erde

E

S E

l S

alva

dor

GC

Gu

lf o

f C

hir

iqu

i

16S

CO

IC

VB

razi

lC

TA

rgJa

pan

Per

uB

PH

awai

iG

uam

Mex

ico

Flo

rida

Syd

ney

Bah

ES

GC

CV

ndash0

081

007

80

083

007

60

080

008

10

081

008

00

074

003

40

074

ndash0

068

007

5B

razi

l0

168

ndash0

062

000

60

067

005

10

054

005

40

054

006

90

073

007

0ndash

004

10

045

CT

016

60

012

ndash0

008

006

50

045

004

70

047

004

70

067

007

10

067

ndash0

038

004

3A

rg0

174

000

80

010

ndash0

069

005

40

056

005

60

056

007

20

075

007

2ndash

004

30

047

Japa

n0

211

015

80

154

015

6ndash

006

10

056

005

60

056

003

40

071

001

7ndash

005

90

068

Per

u0

185

012

60

126

012

60

174

ndash0

006

000

80

006

006

60

081

006

3ndash

005

20

054

BP

016

30

103

010

30

105

016

60

044

ndash0

002

000

00

061

008

10

059

ndash0

052

005

4H

awai

i0

166

010

30

103

010

50

166

004

60

002

ndash0

002

016

20

085

005

9ndash

005

20

056

Gu

am0

163

010

30

103

010

50

166

004

60

000

000

2ndash

016

20

085

005

9ndash

005

30

054

Mex

ico

018

60

144

014

00

138

010

60

164

016

20

061

006

1ndash

006

90

038

ndash0

073

007

7F

lori

da0

066

015

70

155

016

00

192

016

90

157

015

90

157

019

9ndash

006

9ndash

006

10

073

Syd

ney

017

40

133

012

80

131

009

40

152

014

00

140

014

00

122

017

4ndash

ndash0

056

007

2B

ah0

066

015

50

153

015

80

190

016

00

155

015

70

157

020

00

002

017

2ndash

ndashndash

ES

017

10

167

012

10

113

012

30

160

012

70

129

012

90

129

015

50

156

015

2ndash

000

8G

C0

161

011

90

111

012

10

163

012

10

123

012

30

123

016

70

152

015

60

151

000

7ndash







Peru

Panama

HawaiiGuam

84 R COLLIN









86 R COLLIN



DEVELOPMENT











A B

C D

DISCUSSION




88 R COLLIN


Tab

le 4

S

um

mar

y of

Bos

tryc

apu

lus

spec

ies

Dia

gnos

tic

feat

ure

s ar

e h

igh

ligh

ted

in b

old

text

A

bbre

viat

ion

s s

s s

pira

l sc

ulp

ture

B a

cule

atu

sB

gra

visp

inos

us

B c

alyp

trae

form

isB

teg

uli

ciu

sB

pri

tzke

riB

od

ites

B l

ateb

rus

B u

rrac

a

Au

thor

ity

(Gm

elin

179

1)(K

uro

da amp

Hab

e 1

950)

(Des

hay

es 1

830)

(Roc

heb

run

e18

83)

sp n

ov

sp n

ov

sp n

ov

sp n

ov

Fate

of

type

St

Pet

ersb

erg

un

know

nP

aris

Mu

seu

mP

aris

Mu

seu

mA

ust

rali

anM

use

um

Nat

alM

use

um

Fie

ld M

use

um

Fie

ld M

use

um

Typ

e lo

cali

tyM

iddl

eA

mer

ican

Isla

nds

Hir

ado

Is

Nag

asak

iP

ref

Japa

n

Per

u (

dubi

ous)

Sen

egal

Edw

ards

Ree

fS

ydn

ey

Au

stra

lia

Woo

leyrsquo

s P

ool

Cap

e T

own

S

A

La

Paz

BC

SM

exic

oG

ulf

of

Ch

iriq

ui

Pan

ama

Dev

elop

men

tdi

rect

dire

ctp

lan

kto

trop

hic

dire

ct (

from

prot

ocon

ch)

dire

ctd

irec

t w

ith

nu

rse

eggs

dire

ctdi

rect

Egg

siz

e (m

m)

380

(Hoa

glan

d 1

986)

200

(qu

esti

onab

le)

180

ndash53

0ndash56

019

848

837

0

(Am

io 1

963)

Hat

chin

g si

ze(m

m)

840

1000

ndash120

0 38

0ndash

ndashndash

ndash88

8(H

oagl

and

198

6)(I

shik

i 19

36)

Em

bryo

nic

oper

culu

mpr

esen

tndash

pres

ent

ndashab

sen

tpr

esen

tpr

esen

tpr

esen

t

Dis

tin

ct v

elu

mw

ith

foo

dgr

oove

med

ium

spo

tted

w

ith

foo

d gr

oove

ndashla

rge

pig

men

ted

ndashab

sen

tsm

all

un

pigm

ente

dsm

all

un

pigm

ente

dab

sen

t

Em

bryo

nic

sh

ell

scu

lptu

regr

anu

lar

ss

ss a

t h

atch

ing

(Am

io)

fin

e sp

ines

ove

ren

tire

lar

val

shel

l

ndashgr

anu

lar

sssm

ooth

wit

hir

regu

lar

grow

thli

nes

gran

ula

r ss

gran

ula

r ss

Pro

toco

nch

1 w

hor

l1

wh

orl

15

wh

orls

less

th

an 1

w

hor

ln

ot a

vail

able

125

wh

orls

less

th

an 1

w

hor

lle

ss t

han

1w

hor

lL

ocal

itie

sF

lori

da Y

uca

tan

B

aham

asJa

pan

Per

u

Pan

ama

Haw

aii

Gu

amW

est

Afr

ica

Cap

e V

erde

Is

Au

stra

lia

Sou

th A

fric

a

Pat

agon

ia

Bra

zil

La

Paz

Mex

ico

Pan

ama

El

Sal

vado

r










90 R COLLIN
























92 R COLLIN




































94 R COLLIN







































640





96 R COLLIN











A B C D























98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN




















































82 R COLLIN


Tab

le 2

P

airw

ise

Kim

ura

2-p

aram

eter

gen

etic

dis

tan

ces

betw

een

in

divi

dual

s fr

om e

ach

loc

alit

y B

old

valu

es i

ndi

cate

in

tras

peci

fic

com

pari

son

s A

bbre

viat

ion

sA

rg A

rgen

tin

a B

ah B

aham

as

BP

Bay

of

Pan

ama

CT

Cap

e T

own

CV

Cap

e V

erde

E

S E

l S

alva

dor

GC

Gu

lf o

f C

hir

iqu

i

16S

CO

IC

VB

razi

lC

TA

rgJa

pan

Per

uB

PH

awai

iG

uam

Mex

ico

Flo

rida

Syd

ney

Bah

ES

GC

CV

ndash0

081

007

80

083

007

60

080

008

10

081

008

00

074

003

40

074

ndash0

068

007

5B

razi

l0

168

ndash0

062

000

60

067

005

10

054

005

40

054

006

90

073

007

0ndash

004

10

045

CT

016

60

012

ndash0

008

006

50

045

004

70

047

004

70

067

007

10

067

ndash0

038

004

3A

rg0

174

000

80

010

ndash0

069

005

40

056

005

60

056

007

20

075

007

2ndash

004

30

047

Japa

n0

211

015

80

154

015

6ndash

006

10

056

005

60

056

003

40

071

001

7ndash

005

90

068

Per

u0

185

012

60

126

012

60

174

ndash0

006

000

80

006

006

60

081

006

3ndash

005

20

054

BP

016

30

103

010

30

105

016

60

044

ndash0

002

000

00

061

008

10

059

ndash0

052

005

4H

awai

i0

166

010

30

103

010

50

166

004

60

002

ndash0

002

016

20

085

005

9ndash

005

20

056

Gu

am0

163

010

30

103

010

50

166

004

60

000

000

2ndash

016

20

085

005

9ndash

005

30

054

Mex

ico

018

60

144

014

00

138

010

60

164

016

20

061

006

1ndash

006

90

038

ndash0

073

007

7F

lori

da0

066

015

70

155

016

00

192

016

90

157

015

90

157

019

9ndash

006

9ndash

006

10

073

Syd

ney

017

40

133

012

80

131

009

40

152

014

00

140

014

00

122

017

4ndash

ndash0

056

007

2B

ah0

066

015

50

153

015

80

190

016

00

155

015

70

157

020

00

002

017

2ndash

ndashndash

ES

017

10

167

012

10

113

012

30

160

012

70

129

012

90

129

015

50

156

015

2ndash

000

8G

C0

161

011

90

111

012

10

163

012

10

123

012

30

123

016

70

152

015

60

151

000

7ndash







Peru

Panama

HawaiiGuam

84 R COLLIN









86 R COLLIN



DEVELOPMENT











A B

C D

DISCUSSION




88 R COLLIN


Tab

le 4

S

um

mar

y of

Bos

tryc

apu

lus

spec

ies

Dia

gnos

tic

feat

ure

s ar

e h

igh

ligh

ted

in b

old

text

A

bbre

viat

ion

s s

s s

pira

l sc

ulp

ture

B a

cule

atu

sB

gra

visp

inos

us

B c

alyp

trae

form

isB

teg

uli

ciu

sB

pri

tzke

riB

od

ites

B l

ateb

rus

B u

rrac

a

Au

thor

ity

(Gm

elin

179

1)(K

uro

da amp

Hab

e 1

950)

(Des

hay

es 1

830)

(Roc

heb

run

e18

83)

sp n

ov

sp n

ov

sp n

ov

sp n

ov

Fate

of

type

St

Pet

ersb

erg

un

know

nP

aris

Mu

seu

mP

aris

Mu

seu

mA

ust

rali

anM

use

um

Nat

alM

use

um

Fie

ld M

use

um

Fie

ld M

use

um

Typ

e lo

cali

tyM

iddl

eA

mer

ican

Isla

nds

Hir

ado

Is

Nag

asak

iP

ref

Japa

n

Per

u (

dubi

ous)

Sen

egal

Edw

ards

Ree

fS

ydn

ey

Au

stra

lia

Woo

leyrsquo

s P

ool

Cap

e T

own

S

A

La

Paz

BC

SM

exic

oG

ulf

of

Ch

iriq

ui

Pan

ama

Dev

elop

men

tdi

rect

dire

ctp

lan

kto

trop

hic

dire

ct (

from

prot

ocon

ch)

dire

ctd

irec

t w

ith

nu

rse

eggs

dire

ctdi

rect

Egg

siz

e (m

m)

380

(Hoa

glan

d 1

986)

200

(qu

esti

onab

le)

180

ndash53

0ndash56

019

848

837

0

(Am

io 1

963)

Hat

chin

g si

ze(m

m)

840

1000

ndash120

0 38

0ndash

ndashndash

ndash88

8(H

oagl

and

198

6)(I

shik

i 19

36)

Em

bryo

nic

oper

culu

mpr

esen

tndash

pres

ent

ndashab

sen

tpr

esen

tpr

esen

tpr

esen

t

Dis

tin

ct v

elu

mw

ith

foo

dgr

oove

med

ium

spo

tted

w

ith

foo

d gr

oove

ndashla

rge

pig

men

ted

ndashab

sen

tsm

all

un

pigm

ente

dsm

all

un

pigm

ente

dab

sen

t

Em

bryo

nic

sh

ell

scu

lptu

regr

anu

lar

ss

ss a

t h

atch

ing

(Am

io)

fin

e sp

ines

ove

ren

tire

lar

val

shel

l

ndashgr

anu

lar

sssm

ooth

wit

hir

regu

lar

grow

thli

nes

gran

ula

r ss

gran

ula

r ss

Pro

toco

nch

1 w

hor

l1

wh

orl

15

wh

orls

less

th

an 1

w

hor

ln

ot a

vail

able

125

wh

orls

less

th

an 1

w

hor

lle

ss t

han

1w

hor

lL

ocal

itie

sF

lori

da Y

uca

tan

B

aham

asJa

pan

Per

u

Pan

ama

Haw

aii

Gu

amW

est

Afr

ica

Cap

e V

erde

Is

Au

stra

lia

Sou

th A

fric

a

Pat

agon

ia

Bra

zil

La

Paz

Mex

ico

Pan

ama

El

Sal

vado

r










90 R COLLIN
























92 R COLLIN




































94 R COLLIN







































640





96 R COLLIN











A B C D























98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN















































82 R COLLIN


Tab

le 2

P

airw

ise

Kim

ura

2-p

aram

eter

gen

etic

dis

tan

ces

betw

een

in

divi

dual

s fr

om e

ach

loc

alit

y B

old

valu

es i

ndi

cate

in

tras

peci

fic

com

pari

son

s A

bbre

viat

ion

sA

rg A

rgen

tin

a B

ah B

aham

as

BP

Bay

of

Pan

ama

CT

Cap

e T

own

CV

Cap

e V

erde

E

S E

l S

alva

dor

GC

Gu

lf o

f C

hir

iqu

i

16S

CO

IC

VB

razi

lC

TA

rgJa

pan

Per

uB

PH

awai

iG

uam

Mex

ico

Flo

rida

Syd

ney

Bah

ES

GC

CV

ndash0

081

007

80

083

007

60

080

008

10

081

008

00

074

003

40

074

ndash0

068

007

5B

razi

l0

168

ndash0

062

000

60

067

005

10

054

005

40

054

006

90

073

007

0ndash

004

10

045

CT

016

60

012

ndash0

008

006

50

045

004

70

047

004

70

067

007

10

067

ndash0

038

004

3A

rg0

174

000

80

010

ndash0

069

005

40

056

005

60

056

007

20

075

007

2ndash

004

30

047

Japa

n0

211

015

80

154

015

6ndash

006

10

056

005

60

056

003

40

071

001

7ndash

005

90

068

Per

u0

185

012

60

126

012

60

174

ndash0

006

000

80

006

006

60

081

006

3ndash

005

20

054

BP

016

30

103

010

30

105

016

60

044

ndash0

002

000

00

061

008

10

059

ndash0

052

005

4H

awai

i0

166

010

30

103

010

50

166

004

60

002

ndash0

002

016

20

085

005

9ndash

005

20

056

Gu

am0

163

010

30

103

010

50

166

004

60

000

000

2ndash

016

20

085

005

9ndash

005

30

054

Mex

ico

018

60

144

014

00

138

010

60

164

016

20

061

006

1ndash

006

90

038

ndash0

073

007

7F

lori

da0

066

015

70

155

016

00

192

016

90

157

015

90

157

019

9ndash

006

9ndash

006

10

073

Syd

ney

017

40

133

012

80

131

009

40

152

014

00

140

014

00

122

017

4ndash

ndash0

056

007

2B

ah0

066

015

50

153

015

80

190

016

00

155

015

70

157

020

00

002

017

2ndash

ndashndash

ES

017

10

167

012

10

113

012

30

160

012

70

129

012

90

129

015

50

156

015

2ndash

000

8G

C0

161

011

90

111

012

10

163

012

10

123

012

30

123

016

70

152

015

60

151

000

7ndash







Peru

Panama

HawaiiGuam

84 R COLLIN









86 R COLLIN



DEVELOPMENT











A B

C D

DISCUSSION




88 R COLLIN


Tab

le 4

S

um

mar

y of

Bos

tryc

apu

lus

spec

ies

Dia

gnos

tic

feat

ure

s ar

e h

igh

ligh

ted

in b

old

text

A

bbre

viat

ion

s s

s s

pira

l sc

ulp

ture

B a

cule

atu

sB

gra

visp

inos

us

B c

alyp

trae

form

isB

teg

uli

ciu

sB

pri

tzke

riB

od

ites

B l

ateb

rus

B u

rrac

a

Au

thor

ity

(Gm

elin

179

1)(K

uro

da amp

Hab

e 1

950)

(Des

hay

es 1

830)

(Roc

heb

run

e18

83)

sp n

ov

sp n

ov

sp n

ov

sp n

ov

Fate

of

type

St

Pet

ersb

erg

un

know

nP

aris

Mu

seu

mP

aris

Mu

seu

mA

ust

rali

anM

use

um

Nat

alM

use

um

Fie

ld M

use

um

Fie

ld M

use

um

Typ

e lo

cali

tyM

iddl

eA

mer

ican

Isla

nds

Hir

ado

Is

Nag

asak

iP

ref

Japa

n

Per

u (

dubi

ous)

Sen

egal

Edw

ards

Ree

fS

ydn

ey

Au

stra

lia

Woo

leyrsquo

s P

ool

Cap

e T

own

S

A

La

Paz

BC

SM

exic

oG

ulf

of

Ch

iriq

ui

Pan

ama

Dev

elop

men

tdi

rect

dire

ctp

lan

kto

trop

hic

dire

ct (

from

prot

ocon

ch)

dire

ctd

irec

t w

ith

nu

rse

eggs

dire

ctdi

rect

Egg

siz

e (m

m)

380

(Hoa

glan

d 1

986)

200

(qu

esti

onab

le)

180

ndash53

0ndash56

019

848

837

0

(Am

io 1

963)

Hat

chin

g si

ze(m

m)

840

1000

ndash120

0 38

0ndash

ndashndash

ndash88

8(H

oagl

and

198

6)(I

shik

i 19

36)

Em

bryo

nic

oper

culu

mpr

esen

tndash

pres

ent

ndashab

sen

tpr

esen

tpr

esen

tpr

esen

t

Dis

tin

ct v

elu

mw

ith

foo

dgr

oove

med

ium

spo

tted

w

ith

foo

d gr

oove

ndashla

rge

pig

men

ted

ndashab

sen

tsm

all

un

pigm

ente

dsm

all

un

pigm

ente

dab

sen

t

Em

bryo

nic

sh

ell

scu

lptu

regr

anu

lar

ss

ss a

t h

atch

ing

(Am

io)

fin

e sp

ines

ove

ren

tire

lar

val

shel

l

ndashgr

anu

lar

sssm

ooth

wit

hir

regu

lar

grow

thli

nes

gran

ula

r ss

gran

ula

r ss

Pro

toco

nch

1 w

hor

l1

wh

orl

15

wh

orls

less

th

an 1

w

hor

ln

ot a

vail

able

125

wh

orls

less

th

an 1

w

hor

lle

ss t

han

1w

hor

lL

ocal

itie

sF

lori

da Y

uca

tan

B

aham

asJa

pan

Per

u

Pan

ama

Haw

aii

Gu

amW

est

Afr

ica

Cap

e V

erde

Is

Au

stra

lia

Sou

th A

fric

a

Pat

agon

ia

Bra

zil

La

Paz

Mex

ico

Pan

ama

El

Sal

vado

r










90 R COLLIN
























92 R COLLIN




































94 R COLLIN







































640





96 R COLLIN











A B C D























98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN





















































Peru

Panama

HawaiiGuam

84 R COLLIN









86 R COLLIN



DEVELOPMENT











A B

C D

DISCUSSION




88 R COLLIN


Tab

le 4

S

um

mar

y of

Bos

tryc

apu

lus

spec

ies

Dia

gnos

tic

feat

ure

s ar

e h

igh

ligh

ted

in b

old

text

A

bbre

viat

ion

s s

s s

pira

l sc

ulp

ture

B a

cule

atu

sB

gra

visp

inos

us

B c

alyp

trae

form

isB

teg

uli

ciu

sB

pri

tzke

riB

od

ites

B l

ateb

rus

B u

rrac

a

Au

thor

ity

(Gm

elin

179

1)(K

uro

da amp

Hab

e 1

950)

(Des

hay

es 1

830)

(Roc

heb

run

e18

83)

sp n

ov

sp n

ov

sp n

ov

sp n

ov

Fate

of

type

St

Pet

ersb

erg

un

know

nP

aris

Mu

seu

mP

aris

Mu

seu

mA

ust

rali

anM

use

um

Nat

alM

use

um

Fie

ld M

use

um

Fie

ld M

use

um

Typ

e lo

cali

tyM

iddl

eA

mer

ican

Isla

nds

Hir

ado

Is

Nag

asak

iP

ref

Japa

n

Per

u (

dubi

ous)

Sen

egal

Edw

ards

Ree

fS

ydn

ey

Au

stra

lia

Woo

leyrsquo

s P

ool

Cap

e T

own

S

A

La

Paz

BC

SM

exic

oG

ulf

of

Ch

iriq

ui

Pan

ama

Dev

elop

men

tdi

rect

dire

ctp

lan

kto

trop

hic

dire

ct (

from

prot

ocon

ch)

dire

ctd

irec

t w

ith

nu

rse

eggs

dire

ctdi

rect

Egg

siz

e (m

m)

380

(Hoa

glan

d 1

986)

200

(qu

esti

onab

le)

180

ndash53

0ndash56

019

848

837

0

(Am

io 1

963)

Hat

chin

g si

ze(m

m)

840

1000

ndash120

0 38

0ndash

ndashndash

ndash88

8(H

oagl

and

198

6)(I

shik

i 19

36)

Em

bryo

nic

oper

culu

mpr

esen

tndash

pres

ent

ndashab

sen

tpr

esen

tpr

esen

tpr

esen

t

Dis

tin

ct v

elu

mw

ith

foo

dgr

oove

med

ium

spo

tted

w

ith

foo

d gr

oove

ndashla

rge

pig

men

ted

ndashab

sen

tsm

all

un

pigm

ente

dsm

all

un

pigm

ente

dab

sen

t

Em

bryo

nic

sh

ell

scu

lptu

regr

anu

lar

ss

ss a

t h

atch

ing

(Am

io)

fin

e sp

ines

ove

ren

tire

lar

val

shel

l

ndashgr

anu

lar

sssm

ooth

wit

hir

regu

lar

grow

thli

nes

gran

ula

r ss

gran

ula

r ss

Pro

toco

nch

1 w

hor

l1

wh

orl

15

wh

orls

less

th

an 1

w

hor

ln

ot a

vail

able

125

wh

orls

less

th

an 1

w

hor

lle

ss t

han

1w

hor

lL

ocal

itie

sF

lori

da Y

uca

tan

B

aham

asJa

pan

Per

u

Pan

ama

Haw

aii

Gu

amW

est

Afr

ica

Cap

e V

erde

Is

Au

stra

lia

Sou

th A

fric

a

Pat

agon

ia

Bra

zil

La

Paz

Mex

ico

Pan

ama

El

Sal

vado

r










90 R COLLIN
























92 R COLLIN




































94 R COLLIN







































640





96 R COLLIN











A B C D























98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN















































84 R COLLIN









86 R COLLIN



DEVELOPMENT











A B

C D

DISCUSSION




88 R COLLIN


Tab

le 4

S

um

mar

y of

Bos

tryc

apu

lus

spec

ies

Dia

gnos

tic

feat

ure

s ar

e h

igh

ligh

ted

in b

old

text

A

bbre

viat

ion

s s

s s

pira

l sc

ulp

ture

B a

cule

atu

sB

gra

visp

inos

us

B c

alyp

trae

form

isB

teg

uli

ciu

sB

pri

tzke

riB

od

ites

B l

ateb

rus

B u

rrac

a

Au

thor

ity

(Gm

elin

179

1)(K

uro

da amp

Hab

e 1

950)

(Des

hay

es 1

830)

(Roc

heb

run

e18

83)

sp n

ov

sp n

ov

sp n

ov

sp n

ov

Fate

of

type

St

Pet

ersb

erg

un

know

nP

aris

Mu

seu

mP

aris

Mu

seu

mA

ust

rali

anM

use

um

Nat

alM

use

um

Fie

ld M

use

um

Fie

ld M

use

um

Typ

e lo

cali

tyM

iddl

eA

mer

ican

Isla

nds

Hir

ado

Is

Nag

asak

iP

ref

Japa

n

Per

u (

dubi

ous)

Sen

egal

Edw

ards

Ree

fS

ydn

ey

Au

stra

lia

Woo

leyrsquo

s P

ool

Cap

e T

own

S

A

La

Paz

BC

SM

exic

oG

ulf

of

Ch

iriq

ui

Pan

ama

Dev

elop

men

tdi

rect

dire

ctp

lan

kto

trop

hic

dire

ct (

from

prot

ocon

ch)

dire

ctd

irec

t w

ith

nu

rse

eggs

dire

ctdi

rect

Egg

siz

e (m

m)

380

(Hoa

glan

d 1

986)

200

(qu

esti

onab

le)

180

ndash53

0ndash56

019

848

837

0

(Am

io 1

963)

Hat

chin

g si

ze(m

m)

840

1000

ndash120

0 38

0ndash

ndashndash

ndash88

8(H

oagl

and

198

6)(I

shik

i 19

36)

Em

bryo

nic

oper

culu

mpr

esen

tndash

pres

ent

ndashab

sen

tpr

esen

tpr

esen

tpr

esen

t

Dis

tin

ct v

elu

mw

ith

foo

dgr

oove

med

ium

spo

tted

w

ith

foo

d gr

oove

ndashla

rge

pig

men

ted

ndashab

sen

tsm

all

un

pigm

ente

dsm

all

un

pigm

ente

dab

sen

t

Em

bryo

nic

sh

ell

scu

lptu

regr

anu

lar

ss

ss a

t h

atch

ing

(Am

io)

fin

e sp

ines

ove

ren

tire

lar

val

shel

l

ndashgr

anu

lar

sssm

ooth

wit

hir

regu

lar

grow

thli

nes

gran

ula

r ss

gran

ula

r ss

Pro

toco

nch

1 w

hor

l1

wh

orl

15

wh

orls

less

th

an 1

w

hor

ln

ot a

vail

able

125

wh

orls

less

th

an 1

w

hor

lle

ss t

han

1w

hor

lL

ocal

itie

sF

lori

da Y

uca

tan

B

aham

asJa

pan

Per

u

Pan

ama

Haw

aii

Gu

amW

est

Afr

ica

Cap

e V

erde

Is

Au

stra

lia

Sou

th A

fric

a

Pat

agon

ia

Bra

zil

La

Paz

Mex

ico

Pan

ama

El

Sal

vado

r










90 R COLLIN
























92 R COLLIN




































94 R COLLIN







































640





96 R COLLIN











A B C D























98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN



















































86 R COLLIN



DEVELOPMENT











A B

C D

DISCUSSION




88 R COLLIN


Tab

le 4

S

um

mar

y of

Bos

tryc

apu

lus

spec

ies

Dia

gnos

tic

feat

ure

s ar

e h

igh

ligh

ted

in b

old

text

A

bbre

viat

ion

s s

s s

pira

l sc

ulp

ture

B a

cule

atu

sB

gra

visp

inos

us

B c

alyp

trae

form

isB

teg

uli

ciu

sB

pri

tzke

riB

od

ites

B l

ateb

rus

B u

rrac

a

Au

thor

ity

(Gm

elin

179

1)(K

uro

da amp

Hab

e 1

950)

(Des

hay

es 1

830)

(Roc

heb

run

e18

83)

sp n

ov

sp n

ov

sp n

ov

sp n

ov

Fate

of

type

St

Pet

ersb

erg

un

know

nP

aris

Mu

seu

mP

aris

Mu

seu

mA

ust

rali

anM

use

um

Nat

alM

use

um

Fie

ld M

use

um

Fie

ld M

use

um

Typ

e lo

cali

tyM

iddl

eA

mer

ican

Isla

nds

Hir

ado

Is

Nag

asak

iP

ref

Japa

n

Per

u (

dubi

ous)

Sen

egal

Edw

ards

Ree

fS

ydn

ey

Au

stra

lia

Woo

leyrsquo

s P

ool

Cap

e T

own

S

A

La

Paz

BC

SM

exic

oG

ulf

of

Ch

iriq

ui

Pan

ama

Dev

elop

men

tdi

rect

dire

ctp

lan

kto

trop

hic

dire

ct (

from

prot

ocon

ch)

dire

ctd

irec

t w

ith

nu

rse

eggs

dire

ctdi

rect

Egg

siz

e (m

m)

380

(Hoa

glan

d 1

986)

200

(qu

esti

onab

le)

180

ndash53

0ndash56

019

848

837

0

(Am

io 1

963)

Hat

chin

g si

ze(m

m)

840

1000

ndash120

0 38

0ndash

ndashndash

ndash88

8(H

oagl

and

198

6)(I

shik

i 19

36)

Em

bryo

nic

oper

culu

mpr

esen

tndash

pres

ent

ndashab

sen

tpr

esen

tpr

esen

tpr

esen

t

Dis

tin

ct v

elu

mw

ith

foo

dgr

oove

med

ium

spo

tted

w

ith

foo

d gr

oove

ndashla

rge

pig

men

ted

ndashab

sen

tsm

all

un

pigm

ente

dsm

all

un

pigm

ente

dab

sen

t

Em

bryo

nic

sh

ell

scu

lptu

regr

anu

lar

ss

ss a

t h

atch

ing

(Am

io)

fin

e sp

ines

ove

ren

tire

lar

val

shel

l

ndashgr

anu

lar

sssm

ooth

wit

hir

regu

lar

grow

thli

nes

gran

ula

r ss

gran

ula

r ss

Pro

toco

nch

1 w

hor

l1

wh

orl

15

wh

orls

less

th

an 1

w

hor

ln

ot a

vail

able

125

wh

orls

less

th

an 1

w

hor

lle

ss t

han

1w

hor

lL

ocal

itie

sF

lori

da Y

uca

tan

B

aham

asJa

pan

Per

u

Pan

ama

Haw

aii

Gu

amW

est

Afr

ica

Cap

e V

erde

Is

Au

stra

lia

Sou

th A

fric

a

Pat

agon

ia

Bra

zil

La

Paz

Mex

ico

Pan

ama

El

Sal

vado

r










90 R COLLIN
























92 R COLLIN




































94 R COLLIN







































640





96 R COLLIN











A B C D























98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN















































86 R COLLIN



DEVELOPMENT











A B

C D

DISCUSSION




88 R COLLIN


Tab

le 4

S

um

mar

y of

Bos

tryc

apu

lus

spec

ies

Dia

gnos

tic

feat

ure

s ar

e h

igh

ligh

ted

in b

old

text

A

bbre

viat

ion

s s

s s

pira

l sc

ulp

ture

B a

cule

atu

sB

gra

visp

inos

us

B c

alyp

trae

form

isB

teg

uli

ciu

sB

pri

tzke

riB

od

ites

B l

ateb

rus

B u

rrac

a

Au

thor

ity

(Gm

elin

179

1)(K

uro

da amp

Hab

e 1

950)

(Des

hay

es 1

830)

(Roc

heb

run

e18

83)

sp n

ov

sp n

ov

sp n

ov

sp n

ov

Fate

of

type

St

Pet

ersb

erg

un

know

nP

aris

Mu

seu

mP

aris

Mu

seu

mA

ust

rali

anM

use

um

Nat

alM

use

um

Fie

ld M

use

um

Fie

ld M

use

um

Typ

e lo

cali

tyM

iddl

eA

mer

ican

Isla

nds

Hir

ado

Is

Nag

asak

iP

ref

Japa

n

Per

u (

dubi

ous)

Sen

egal

Edw

ards

Ree

fS

ydn

ey

Au

stra

lia

Woo

leyrsquo

s P

ool

Cap

e T

own

S

A

La

Paz

BC

SM

exic

oG

ulf

of

Ch

iriq

ui

Pan

ama

Dev

elop

men

tdi

rect

dire

ctp

lan

kto

trop

hic

dire

ct (

from

prot

ocon

ch)

dire

ctd

irec

t w

ith

nu

rse

eggs

dire

ctdi

rect

Egg

siz

e (m

m)

380

(Hoa

glan

d 1

986)

200

(qu

esti

onab

le)

180

ndash53

0ndash56

019

848

837

0

(Am

io 1

963)

Hat

chin

g si

ze(m

m)

840

1000

ndash120

0 38

0ndash

ndashndash

ndash88

8(H

oagl

and

198

6)(I

shik

i 19

36)

Em

bryo

nic

oper

culu

mpr

esen

tndash

pres

ent

ndashab

sen

tpr

esen

tpr

esen

tpr

esen

t

Dis

tin

ct v

elu

mw

ith

foo

dgr

oove

med

ium

spo

tted

w

ith

foo

d gr

oove

ndashla

rge

pig

men

ted

ndashab

sen

tsm

all

un

pigm

ente

dsm

all

un

pigm

ente

dab

sen

t

Em

bryo

nic

sh

ell

scu

lptu

regr

anu

lar

ss

ss a

t h

atch

ing

(Am

io)

fin

e sp

ines

ove

ren

tire

lar

val

shel

l

ndashgr

anu

lar

sssm

ooth

wit

hir

regu

lar

grow

thli

nes

gran

ula

r ss

gran

ula

r ss

Pro

toco

nch

1 w

hor

l1

wh

orl

15

wh

orls

less

th

an 1

w

hor

ln

ot a

vail

able

125

wh

orls

less

th

an 1

w

hor

lle

ss t

han

1w

hor

lL

ocal

itie

sF

lori

da Y

uca

tan

B

aham

asJa

pan

Per

u

Pan

ama

Haw

aii

Gu

amW

est

Afr

ica

Cap

e V

erde

Is

Au

stra

lia

Sou

th A

fric

a

Pat

agon

ia

Bra

zil

La

Paz

Mex

ico

Pan

ama

El

Sal

vado

r










90 R COLLIN
























92 R COLLIN




































94 R COLLIN







































640





96 R COLLIN











A B C D























98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN


















































A B

C D

DISCUSSION




88 R COLLIN


Tab

le 4

S

um

mar

y of

Bos

tryc

apu

lus

spec

ies

Dia

gnos

tic

feat

ure

s ar

e h

igh

ligh

ted

in b

old

text

A

bbre

viat

ion

s s

s s

pira

l sc

ulp

ture

B a

cule

atu

sB

gra

visp

inos

us

B c

alyp

trae

form

isB

teg

uli

ciu

sB

pri

tzke

riB

od

ites

B l

ateb

rus

B u

rrac

a

Au

thor

ity

(Gm

elin

179

1)(K

uro

da amp

Hab

e 1

950)

(Des

hay

es 1

830)

(Roc

heb

run

e18

83)

sp n

ov

sp n

ov

sp n

ov

sp n

ov

Fate

of

type

St

Pet

ersb

erg

un

know

nP

aris

Mu

seu

mP

aris

Mu

seu

mA

ust

rali

anM

use

um

Nat

alM

use

um

Fie

ld M

use

um

Fie

ld M

use

um

Typ

e lo

cali

tyM

iddl

eA

mer

ican

Isla

nds

Hir

ado

Is

Nag

asak

iP

ref

Japa

n

Per

u (

dubi

ous)

Sen

egal

Edw

ards

Ree

fS

ydn

ey

Au

stra

lia

Woo

leyrsquo

s P

ool

Cap

e T

own

S

A

La

Paz

BC

SM

exic

oG

ulf

of

Ch

iriq

ui

Pan

ama

Dev

elop

men

tdi

rect

dire

ctp

lan

kto

trop

hic

dire

ct (

from

prot

ocon

ch)

dire

ctd

irec

t w

ith

nu

rse

eggs

dire

ctdi

rect

Egg

siz

e (m

m)

380

(Hoa

glan

d 1

986)

200

(qu

esti

onab

le)

180

ndash53

0ndash56

019

848

837

0

(Am

io 1

963)

Hat

chin

g si

ze(m

m)

840

1000

ndash120

0 38

0ndash

ndashndash

ndash88

8(H

oagl

and

198

6)(I

shik

i 19

36)

Em

bryo

nic

oper

culu

mpr

esen

tndash

pres

ent

ndashab

sen

tpr

esen

tpr

esen

tpr

esen

t

Dis

tin

ct v

elu

mw

ith

foo

dgr

oove

med

ium

spo

tted

w

ith

foo

d gr

oove

ndashla

rge

pig

men

ted

ndashab

sen

tsm

all

un

pigm

ente

dsm

all

un

pigm

ente

dab

sen

t

Em

bryo

nic

sh

ell

scu

lptu

regr

anu

lar

ss

ss a

t h

atch

ing

(Am

io)

fin

e sp

ines

ove

ren

tire

lar

val

shel

l

ndashgr

anu

lar

sssm

ooth

wit

hir

regu

lar

grow

thli

nes

gran

ula

r ss

gran

ula

r ss

Pro

toco

nch

1 w

hor

l1

wh

orl

15

wh

orls

less

th

an 1

w

hor

ln

ot a

vail

able

125

wh

orls

less

th

an 1

w

hor

lle

ss t

han

1w

hor

lL

ocal

itie

sF

lori

da Y

uca

tan

B

aham

asJa

pan

Per

u

Pan

ama

Haw

aii

Gu

amW

est

Afr

ica

Cap

e V

erde

Is

Au

stra

lia

Sou

th A

fric

a

Pat

agon

ia

Bra

zil

La

Paz

Mex

ico

Pan

ama

El

Sal

vado

r










90 R COLLIN
























92 R COLLIN




































94 R COLLIN







































640





96 R COLLIN











A B C D























98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN















































88 R COLLIN


Tab

le 4

S

um

mar

y of

Bos

tryc

apu

lus

spec

ies

Dia

gnos

tic

feat

ure

s ar

e h

igh

ligh

ted

in b

old

text

A

bbre

viat

ion

s s

s s

pira

l sc

ulp

ture

B a

cule

atu

sB

gra

visp

inos

us

B c

alyp

trae

form

isB

teg

uli

ciu

sB

pri

tzke

riB

od

ites

B l

ateb

rus

B u

rrac

a

Au

thor

ity

(Gm

elin

179

1)(K

uro

da amp

Hab

e 1

950)

(Des

hay

es 1

830)

(Roc

heb

run

e18

83)

sp n

ov

sp n

ov

sp n

ov

sp n

ov

Fate

of

type

St

Pet

ersb

erg

un

know

nP

aris

Mu

seu

mP

aris

Mu

seu

mA

ust

rali

anM

use

um

Nat

alM

use

um

Fie

ld M

use

um

Fie

ld M

use

um

Typ

e lo

cali

tyM

iddl

eA

mer

ican

Isla

nds

Hir

ado

Is

Nag

asak

iP

ref

Japa

n

Per

u (

dubi

ous)

Sen

egal

Edw

ards

Ree

fS

ydn

ey

Au

stra

lia

Woo

leyrsquo

s P

ool

Cap

e T

own

S

A

La

Paz

BC

SM

exic

oG

ulf

of

Ch

iriq

ui

Pan

ama

Dev

elop

men

tdi

rect

dire

ctp

lan

kto

trop

hic

dire

ct (

from

prot

ocon

ch)

dire

ctd

irec

t w

ith

nu

rse

eggs

dire

ctdi

rect

Egg

siz

e (m

m)

380

(Hoa

glan

d 1

986)

200

(qu

esti

onab

le)

180

ndash53

0ndash56

019

848

837

0

(Am

io 1

963)

Hat

chin

g si

ze(m

m)

840

1000

ndash120

0 38

0ndash

ndashndash

ndash88

8(H

oagl

and

198

6)(I

shik

i 19

36)

Em

bryo

nic

oper

culu

mpr

esen

tndash

pres

ent

ndashab

sen

tpr

esen

tpr

esen

tpr

esen

t

Dis

tin

ct v

elu

mw

ith

foo

dgr

oove

med

ium

spo

tted

w

ith

foo

d gr

oove

ndashla

rge

pig

men

ted

ndashab

sen

tsm

all

un

pigm

ente

dsm

all

un

pigm

ente

dab

sen

t

Em

bryo

nic

sh

ell

scu

lptu

regr

anu

lar

ss

ss a

t h

atch

ing

(Am

io)

fin

e sp

ines

ove

ren

tire

lar

val

shel

l

ndashgr

anu

lar

sssm

ooth

wit

hir

regu

lar

grow

thli

nes

gran

ula

r ss

gran

ula

r ss

Pro

toco

nch

1 w

hor

l1

wh

orl

15

wh

orls

less

th

an 1

w

hor

ln

ot a

vail

able

125

wh

orls

less

th

an 1

w

hor

lle

ss t

han

1w

hor

lL

ocal

itie

sF

lori

da Y

uca

tan

B

aham

asJa

pan

Per

u

Pan

ama

Haw

aii

Gu

amW

est

Afr

ica

Cap

e V

erde

Is

Au

stra

lia

Sou

th A

fric

a

Pat

agon

ia

Bra

zil

La

Paz

Mex

ico

Pan

ama

El

Sal

vado

r










90 R COLLIN
























92 R COLLIN




































94 R COLLIN







































640





96 R COLLIN











A B C D























98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN
























































90 R COLLIN
























92 R COLLIN




































94 R COLLIN







































640





96 R COLLIN











A B C D























98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN















































90 R COLLIN
























92 R COLLIN




































94 R COLLIN







































640





96 R COLLIN











A B C D























98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN


























































92 R COLLIN




































94 R COLLIN







































640





96 R COLLIN











A B C D























98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN















































92 R COLLIN




































94 R COLLIN







































640





96 R COLLIN











A B C D























98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN



































































94 R COLLIN







































640





96 R COLLIN











A B C D























98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN















































94 R COLLIN







































640





96 R COLLIN











A B C D























98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN

































































640





96 R COLLIN











A B C D























98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN















































96 R COLLIN











A B C D























98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN





































































98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN















































98 R COLLIN
















ACKNOWLEDGEMENTS





REFERENCES






























100 R COLLIN


















































REFERENCES






























100 R COLLIN















































100 R COLLIN




















































Documents

Development, phylogeny, and taxonomy of Bostrycapulus