Matton AoBRe stNKie
Nahe A AD NERS
ARAM nahn

ea
Se eer

Bei Muianttinncny

aot pane a ee

ne eaten nen
ae

See

Soares
adie

parabubedith nek heaton

PNA alee Note aninee nee

SPAS aoe,
i Genie . wean
EG WH a \ \

“eat

ts

PERE aI E ERM PIC VELARDE? nh Ca de comer NEN ome pervert Mee Bi! RIMINI INE LD SIVIE ET EOWEEEENES bua Fee we oe SUNS Pa Peet ete wt SS FRE ts Eee te

- = un Z Un = as = zZ
= 2) o 2 aos] ° wo NS °
a = 2 5 2 5 > WS §£
‘ =) 5 ~ F sv RK, =)
ar = z Ein% = Ee casa \ -
= e = a - 2 . tate
_ Zz o z D Zz Hs —£
SMITHSONIAN INSTITUTION _ NOILALILSNI S31YVYUEIT_ LIBRARIES SMITHSONIAN INSTITUTIO
7) z es 7) z o z ” z :
= ey ee < = Z£ Me = =< @®&,.
= = Sj ae hy Mare = Z WS | z 5
5 9 WS i Jf : ae a Nae BMS
e) 4 w o A
E : 2 Oy * 3 ENG 2 z
ue a ee a 2 a . 2 2
HABE) LSU ell aPU Esper Htc) REM ea EDT USCS ater) La TS I SiS ota os NVINOSHLIWS S3I1YVEE
” 2 2” — s WN
< 2 4 =. it fy = 2 2 WS =
z < 2 “¢ If 2 < 2 WO =
o ox 4
= oO = an YY = ry = i YS e
2 ce eis 2 a Fe a rea ey
RARIES SMITHSONIAN_INSTITUTION NOILNILILSNI SA!ly¥vVugiT LIBRARIES SMITHSONIAN_INSTITUTIC
z eS eS = 2 Ds rs zs Ds
—_ iso) — oO == — V/; jee]
a ed E 2 = 50 5 Gy, 20
= “> = > = > = YE ff >
Be : b b : iY fi ®
z o z a = o z o

[INLILSNI NYVINOSHLIWNS S31yvugit LIBRARIES SMITHSONIAN INSTITUTION NOILNLILSNI_ NWINOSHLIWS
% V4

Y flow Gy : \ MS

RARIES SMITHSONIAN INSTITUTION NOILALILSNI_NVINOSHLINS S31¥YVYSIT LIBRARIES

N.

SMITHSONIAN
NVINOSHLIWS
SMITHSONIAN
NVINOSHLIIWS

SMITHSONIAN
yy
NWINOSHLIWS

LIBRAR! ES SMITHSONIAN
NVINOSHLIINS

SMITHSONIAN INSTITUTIO

Uy,

LIBRARIES
NOILALILSNI
LIBRARIES
NOILALILSNI
NOILNLILSN!
AS
NOILNLILSNI

LNLILSNI NVINOSHLINS S3!IYVYUGIT LIBRARIES SMITHSONIAN INSTITUTION NOILNLILSNI NVINOSHLINS S31luVud

Sa1yvugdit LIBRARIES

Saiuvyall
INSTITUTION
saliyuvuagit
INSTITUTION
INSTITUTION
@; Ge
INSTITUTION

RARIES SMITHSONIAN INSTITUTION. NOILNLILSNI NVINOSHLINS S3IUVHSIT LIBRARIES
Se z
SQ

INLILSNI NVINOSHLIWS

SMITHSONIAN INSTITUTIC

NVINOSHLINS S3iuvuagit

NVINOSHLIWS
SMITHSONIAN
NVINOSHLIWS
BK
SY
SMITHSONIAN
Vil
SMITHSONIAN

CLA
NVINOSHLIWS

*

saiuvugi LIBRARIES SMITHSONIAN INSTITUTION NO[LNLILSNI NVINOSHLIWS saluvug

LIBRARIES

NOILNLILSNI
NOILNLILSNI

2

3RARIES_ SMITHSONIAN

NOILALILSNI

INSTITUTION NOILNLILSNI Saiuvyudi

4
X
YP My;
QS fe
i7_ LIBRARIES

saiuvua

\ LD: f)
saruvugi LIBRARIES SMITHSONIAN

INSTITUTION NOILALILSNI

INSTITUTION
INSTITUTION
INSTITUTION
S3i1yvyds4

JNLILSNI NVINOSHLINS S31Y¥VYSIT INSTITUTION NOILNLILSNI NVINOSHLINS S31uVudl

Ee

NVINOSHLIWS Saiyvydit LIBRARIES

SMITHSONIAN
NVINOSHLIWS
‘SMITHSONIAN
SMITHSONIAN
NVINOSHLIWS

SMITHSONIAN
ty tlie
NVINOSHLIWS

|
)
}
)
).
)
)
J
}

CD a fo a

RARIES SMITHSONIAN INSTITUTION NOILNLILSNI NVINOSHLIWS — Ssaluvuad ae LIBRARI ES” SMITHSONIAN INSTITUTIOI

6 = S a z 5 e S
= oO = o 2) o 2) =
= 4 > ~ ad o = a 5 eu
E = > = > Es >
raat aL = D — 0) = D
a ie = - a 5 2
= ys z mn 2 WD Zz m
= = = yn — 69)
SAIYVYEIT LIBRARIES SMITHSONIAN INSTITUTION NOILOLILSNI
= ge = we: ¢ z wa 2) Zz 7)
.< = ses we < N = <x =
= = wt, gh Z ‘ Zz SAY Ns = z 4 'Z =
D d Uh 2 \S B wo: g BS
z= Gy = \ 2 = g z o?
= > z = > S > = >
a z a eee a ~ 5 2
SMITHSONIAN _INSTITUTION NOILALILSNI NVINOSHLINS S3IYVYSIT LIBRARI ES SMITHSONIAN INSTITUTIO!
a Zz Me Be ve Z ee 2
uJ 2” m S\N eR uj {es}
a. “a 0 4 AWS o = = / fp 3
a: a < a ¥ SS Notes a S I
: : e eS = é SGisy §
a “We 3 = 5 et 5 ee S
a A z = 2 Senay z ay 5 z
CNVINOSHLIWS _S3 1yYVvug aa LIBRARI ES_ SMITHSONIAN INSTITUTION — NOILMLILSNI_NVINOSHLINS — $3 1Yvy gl
— = — iy = — ~
a = wo o je o \, S
> = > = <> = > WX =
2 re = 2 = WOW E
= e Zz E. aie = ae NC
S iB RNS z ma 2 im Z m <N z
Es = = wo = wn eee =
RAR I ES, MITHSONIAN INSTITUTION NOILNIILSNI ~NVINOSHIIWS S32 tYvVugit aE BRARI ES SMITHSONIAN
= & ~~ = s = = ne , ze “we = 2
=j = \, = 4; = = Wh = = z
= 5S WSN 2 77243 5 Yu O 5 8
fo} T WWE SG Vy ae o = O =
= Ee \ 2%” = z = z Ee
= UN >" = >" = \ > =
rs ” “ge 2 wo re wo cS Fa cra
_NVINOSHLINS SASIYVHYAIT LIBRARIES SMITHSONIAN INSTITUTION NOILNLILSNI NYINOSHLINS $3 1YVvygl
Zz 2 > ve) = ” = ”
nv a 77) ea o e (es =
5 oe = a hy = oc = Xs a
Cc pie S ss we s e AS =
= oa ral e = 5 a ONE
2 z 2 = = as
a 2 a a
" SSeS NSm tI TION NOILNLILSNI NVINOSHLINS S3IYVYEIT LIBRARIES SMITHSONIAN INSTITUTIOI!
ae z & z - Zz 7
2 ace 2 = ° o 2 Oo
(= By, > = > ° = > Se >
E * a = a) = ee) = D
79) ” = ” am w ee
z ah Zz iy z iB z Oo
ENLILSNI et SVE RISLIBRARIES ag p NOILNLILSNI B
o: z
< = < = < = =
= A eh oe =) = = =
2 2 iy * 2 = 2° eo
a 2 e » 8 = = S

SMITHSONIAN _INSTITUTIO?

RARIES SMITHSONIAN INSTITUTION NOILNLILSNI LIBRARIES

S

=
2
Sia
Oo
id)
a
=
[ép)
2) i Z a z us a
xe.t~t¢% 7 A © eal a = o =
PU) 3 < : : : S :
« Dy 4 ee = Pe = eS =
0 Ub & a 5 E 5 = S
LNLIISNI_NVINOSHLINS “S3IUVYSIT LIBRARIES— ~ INSTITUTION NOILNLILSNI_NVINOSHLIWS Sal uvu gt
ae Zz ss
o = iy = 2 = SE. =
. é 5 2 E 2 Ne 5
> = > = “> = gn Ya WSS es
@ = z 2 E = NOW 5
A oO = ” = ” SS =
i wn ies z ws = a 2 D ane &
RARIES SMITHSONIAN INSTITUTION NOILMLILSNI NVINOSHLIWS LIBRARIES SMITHSONIAN INSTITUTION
{ Z aliig a) ; z o Ze oe Y a
= ee = 4 yy, < = < = =
4 Pd X& ar) ny Pe, s < = A
a “ayy <
AE : Na z YG z 2 WS 2 2
myer 2 iS ANS Ze eats Z E Wy 2 =
. = =i cal YAS >
aN 2 7 oS z e 2 B * =. a 1

LILSNI_ NVINOSHLINS S31YVUGIT LIBRARIES SMITHSONIAN INSTITUTION NOILNLILSNI. NVINOSHLINS Saluvyal:

:

Hels

VELIGER

A Quarterly published by

CALIFORNIA MALACOZOOLOGICAL SOCIETY, INC.
Berkeley, California

R. Stohler, Founding Editor

Volume 30

July 1, 1987 to April 1, 1988

TABLE OF CONTENTS
Number 1 (July 1, 1987)

In Memoriam: Sir Maurice Yonge, F.R.S. 1946; C.B.E. 1954;
Kt. 1967.
Jor” W. HEDGPETH
The maintenance of polymorphism and cryptic mimesis in the
limpet Scurria variabilis by two species of Cinclodes (Aves:
Furnariinae) in central Chile.
PuiLip A. R. Hockey, ALISON L. BOSMAN, AND PETER G.
RYAN 5
Seasonal growth patterns in the tropical littorinid snails Littorina
angulifera and Tectarius muricatus.
Jerr M. BurGETT, JOHN D. CuBiIT, AND RICARDO C.

WBEIOMPSON( 35 seal ote! tek oranone aed nee ROE 11

Courtship and dart shooting behavior of the land snail Helix
aspersa.

IDARTIGL Jo ID). (CiSMWING cocscacedsgcucoyneonssvnges 24

Ecology and burrowing behavior of Ascobulla ulla (Opisthobran-
chia: Ascoglossa).
ID WANDS, 185 ID, INVIIIT . . Scescascosceavvavecseonse 40
Cryptomya californica (Conrad, 1837): observations on its habitat,
behavior, anatomy, and physiology.
EDWIN V. LAWRY 46
Gametogenesis and reproductive cycle of the surf clam Mesodesma
donacium (Lamarck, 1818) (Bivalvia: Mesodesmatidae) at
Queule Beach, southern Chile.
SANTIAGO PEREDO, ESPERANZA PARADA, AND IVAN

WALDEBENIT Om cen eas Nee cad ee Ae 55
Oxygen uptake and the effect of feeding in Nautilus.
IMU J's WIRES! 25 ache eee ia ee oe ea ee 69

The Indo-West Pacific species of the genus 7rigonostoma sensu
stricto (Gastropoda: Cancellariidae).

RICHARD E. PETIT AND M. G. HARASEWYCH ........ 76
Two new aeolid nudibranchs from southern California.
DAVID) WO BEHRENS: 235. oe ge De ee 82

First records of the pteropods Clio scheelei (Munthe, 1888) and
Cho andreae (Boas, 1886) (Opisthobranchia: Thecosomata)
from the western Pacific Ocean.

L. J. NEWMAN AND J. G. GREENWOOD ............. 90

Mass mortality of the bubble snail Bulla gouldiana Pilsbry, 1893
(Gastropoda: Opisthobranchia).

TUMONNEHY ID), STORENG 5420 0cccoscasagacunonsscos 95

“Punctum pusillum” (Gastropoda: Pulmonata: Punctidae)—a
correction.

BARRY: RODH 2) BRE e ght ter, Hie etree Peet oe ee 95

Synonymy of Rabdotus sonorensis (Pilsbry, 1928) with Rabdotus
nigromontanus (Dall, 1897) (Gastropoda: Pulmonata: Bu-
limulidae).

JAMS 18, IG ONIVINN, 5.5 0bcs0doganccaacvaccccncas 96

Range extension for Doridella steinbergae (Lance, 1962) to Prince
William Sound, Alaska.

INNORAUR FOSTERS 53.5 cn ce oes ear eee eee 97

Hermaea vancouverensis O’ Donoghue, 1924, from Kodiak Island
and Unga Island, Alaska.

INORA’R. FOSEER (as sats ayn oe ee 98

Pinna rugosa Sowerby, 1835 (Bivalvia: Pinnidae) at the Gala-
pagos Islands.

Number 2 (October 1, 1987)

Deep-sea gastropods of the genus Aforia (Turridae) of the Pacific:
species composition, systematics, and functional morphology
of the digestive system.

A. V. SYSOEV AND YU. I. KANTOR 105

The effects of aggregation and microhabitat on desiccation and
body temperature of the black turban snail, Tegula funebralis
(A. Adams, 1855).

KAREN E. MARCHETTI AND JONATHAN B. GELLER.... 127

Behavioral control of water loss in the terrestrial slug Deroceras
reticulatum (Muller): body-size constraints.

Tuomas A. WAITE 134

Responses of a mussel to shell-boring snails: defensive behavior
in Mytilus edulis?

ATRETOMIAS CAG VWIAWIN Bit sdeccci cc satire oor cherie ea eee 138

Skeletal growth histories of Protothaca staminea (Conrad) and
Protothaca grata (Say) throughout their geographic ranges,
northeastern Pacific.

IROWITRD Ifo ISUNIAINCWON «oes cccscucesccscceacacce 148

Age and growth of the subantarctic limpet Nacella (Patinigera)
magellanica magellanica (Gmelin, 1791) from the Strait of
Magellan, Chile.

LEONARDO F. GUZMAN AND CarLos F. RIos

il

YiVESCINET =. 52. occu situs o 8d bost ae hg sae ae 98
Herbivory in juvenile //yanassa obsoleta (Neogastropoda).
(GAYEVAC OB RIEN CETTE RVs ese eee a eee 167

Starvation metabolism in the cerithiids Cerithidea (Cerithideop-
silla) cingulata (Gmelin) and Cerithium coralium Kiener.
Y. PRABHAKARA Rao, V. UMA DEVI, AND D. G. V. PRASADA
RAo 173
A new and polytypic species of Helminthoglypta (Gastropoda:
Pulmonata) from the Transverse Ranges, California.
BARRY ROTH 184
A new species of Naquetia (Muricidae) from the Gulf of Aqaba.
ANTHONY D’ATTILIO AND CAROLE M. HERTZ 190
Pyropeltidae, a new family of cocculiniform limpets from hy-
drothermal vents.

JAMES H. MCLEAN AND GERHARD HASZPRUNAR ..... 196
Fact or artifact?

Se VAN PD DERYSPOEL tras oath es oe eae 206
Response to “Fact or Artifact?” by S. van der Spoel.

RONALDEW|GIEMERG aa) ee eat ee ree 207

Number 3 (January 4, 1988)

The functional morphology of scaphopod captacula.
INORNLD Iky, SUMONS. pu onoepavousecanoneoeaa nate 213
Ontogenic change in the radula of the gastropod Epztonium bil-
leeana (Prosobranchia: Epitoniidae).
ANDREW J. PAGE AND RICHARD C. WILLAN 222
Illustrated embryonic stages of the eastern Atlantic squid Loligo

Jorbesu.
S. SEGAWA, W. T. YANG, H.-J. MARTHY, AND R. T.
JBUNINIOOIN, 5 co. hata ake ote. ig eet nee me reanent feta ae 230
The red foot of a lepidopleurid chiton: evidence for tissue hemo-
globins.

Douc.as J. EERNISSE, NorA B. TERWILLIGER, AND ROBERT
(Oi), TUS RWNABET (CISL sono podera-cio-e ged aco evasion a eae 244
Chromosomes of some subantarctic brooding bivalve species.
CATHERINE THIRIOT-QUIEVREUX, JACQUES SOYER, MARC
Bouvy, AND JOHN A. ALLEN 248
Reproduction and growth of the brooding bivalve 77ransennella
tantilla.
Mary ANN ASSON-BATRES 257
Aspects of the life history and population biology of Notospisula
trigonella (Bivalvia: Mactridae) from the Hawkesbury Es-
tuary, southeastern Australia.
A. R. JONES, A. MurRRAY, AND G. A. SKILLETER

Reproduction in a brackish-water mytilid: gametogenesis and
embryonic development.
R. T. F. BERNARD, B. R. DAVIES, AND A. N. HODGSON ...

Sicrtilidey Mootle eat Soyo a aNeENCae: bya alka cena etaeche eae 278

Effect of eyestalk ablation on oviposition in the snail Lymnaea
acuminata.

S. K. SINGH AND R. A. AGARWAL ................- 291

A review of the genus Agaronia (Olividae) in the Panamic prov-
ince and the description of two new species from Nicaragua.
AL LOPEZ, MICHEL MONTOYA, AND JULIO LOPEZ .. 295
A review of the generic divisions within the Phyllidiidae with
the description of a new species of Phyllidiopsis (Nudibran-
chia: Phyllidiidae) from the Pacific ‘coast of North America.
TERRENCE M. GOSLINER AND DaviD W. BEHRENS.... 305
A new species of Gastropteron (Gastropoda: Opisthobranchia)
from Reunion Island, Indian Ocean.
TERRENCE M. GOSLINER AND GARY C. WILLIAMS .... 315
The first record of Polycerella Verrill, 1881, from the Pacific,
with the description of a new species.
DaviD W. BEHRENS AND TERRENCE M. GOSLINER.... 319
Anatomical information on Thorunna (=Babaina) (Nudibranchia:
Chromodorididae) from Toyama Bay and vicinity, Japan.
KIKUTARO BaBA 325

Number 4 (April 1, 1988)

The possible rdéle of gut bacteria in nutrition and growth of the
sea hare Aplysia.
Timotuy Z. VITALIS, MARGOT J. SPENCE, AND THOMAS H.
CAREFOOT 333
Penetration of the radial hemal and perihemal systems of Linckia
laevigata (Asteroidea) by the proboscis of Thyca crystallina,
an ectoparasitic gastropod.
D. A. EGLorrF, D. T. SMOUSE, JR., AND J. E. PEMBROKE ..
sl Aa ANS co te A cole ARE akEN rPO e 342
Gastric contents of Fissurella maxima (Mollusca: Archeogastro-
poda) at Los Vilos, Chile.
CECILIA Osorio, M. ELIANA RAMIREZ, AND JENNIE
SALGADO 347
Variable population structure and tenacity in the intertidal chiton
Katharina tunicata (Mollusca: Polyplacophora) in northern
California.
TIMOTHY D. STEBBINS 351
Observations on the larval and post-metamorphic life of Con-
cholepas concholepas (Bruguiére, 1789) in laboratory culture.
Louis H. D1SALvo 358
Spawning and larval development of the trochid gastropod Cal-
hiostoma higatum (Gould, 1849).

ALAN R. HOLYOAK 369
Individual movement patterns of the minute land snail Punctum
pygmaeum (Draparnaud) (Pulmonata: Endodontidae).

ANETTE BAUR AND BRUNO BAUR

372

The gastropods in the streams and rivers of five Fiji Islands:
Vanua Levu, Ovalau, Gau, Kadavu, and Taveuni.

7 Sep LLAVINES taal ties ani cc iS are A ker sisal pe neg yg~iuet SHY
New molluscan hosts for two shrimps and two crabs on the coast
of Baja California, with some remarks on distribution.

ERNESTO CAMPOS-GONZALEZ

384

ill

Systematics of the Scurriini (new tribe) of the northwestern Pa-
cific Ocean (Patellogastropoda: Lottiidae).
Davip R. LINDBERG 387
Anatomy and zoogeography of Glossodoris sedna and Chromodoris
grahami (Opisthobranchia: Nudibranchia) in the tropical
western Atlantic and Caribbean.
HANS BERTSCH 395
A new fossil Cypraea (Gastropoda: Prosobranchia) from southern
Africa with notes on the Alexandria Formation.
WILLIAM R. LILTVED AND F. G. LE Roux 400
Two new species of Liotiinae (Gastropoda: Turbinidae) from
the Philippine Islands.
JAMBSUEIIMIGISEANE scape se ony Sere es oe 408
Six new species of Terebridae (Mollusca: Gastropoda) from Pan-
ama and the Indo-West Pacific.
TWILA BRATCHER 412
Assignment of genus Naesvotus (Albers, 1850) of several species
formerly assigned to Rabdotus (Albers, 1850) (Gastropoda:
Pulmonata: Bulimulidae).
JAMES E. HOFFMAN 417
Mexichromis tura: range extension of a rarely observed nudi-
branch.
ALEX KERSTITCH AND HANS BERTSCH.............. 421
New record of the coral clam Coralliophaga coralliophaga (Gmelin,
1791) (Bivalvia: Trapezidae) in the Mediterranean Sea.
CARMEN SALAS, AGUSTIN BARRAJON, AND FRANCISCO

GIARIPENAE oat ha euro nan eeee ieen mnegie ccc oe 421
Harpidae Bronn, 1849 (Gastropoda): conserved by ICZN.
WILLIAM K. EMERSON AND ROGER N. HUGHES ...... 422
A note on unjustified emendations.
RUDIGEREBIBEERG. 4) tls ase aie a 423
Note on Leaflets in Malacology.
RICHARD Ey DEM en aeie sy Sean eae ee fo 424

AUTHOR INDEX

(AGARIWATEO Roe Ang | Faen Uy ree amen et tat enemy ere Aenean 291
AEE NGS] clei oot ae car tanct aca sci henen ee Mee ete Peer 248
ASSON-BATRES, M. A.............. Pade Ree et es aa DDT/
BAB Aves Kraan 2 ete 5 298 wire scape Me one Stitt Pee oe gt oy. oe OR 325
YAR RINTON SAG Ate ce eee yee ir cece ee ere 421
BYAURG HAG re Oo sec Bien. Re bon 8 = eae oe, Saat Loe 372
IBAURGM ES erie cate Oe 2 nye oO aA eS, a ee 372
BEHRENS aD S Wie rs one-car hones crea aes 82, 305, 319
IBERINARID a ies elena bnr 228 SUS os ly er etc ee ee ee 278
IBERDSCH whe eer a oes (102), (103), (331), 395, 421
IBIRTEE RS Rae cee erent ee fe.) nape ee Gee eee eee 423
IBOSNTANIS AS Ee ocr ces Sy cies rate ee Ree ee en 5
BOUNNS IMIS can, ne 5 i ee Bee) ee 248
BRATCHERS Le 23 oc hrc fo toe Ae en ee 412
BRENCHTEEVASG- Acs) 8 20902 2 SER Stee 3 ve verter ae 167
BURGERDS Ji. NB ca ete oe eee ea Oe eter ee let
GAMPOS=-< GONZALEZ) 5 een ee ee eee 384
GAREFOOT:. (Ds Fn oe Be Ge as See ee ee en oe 335)
GARBENA SE Sears ek ae ae te Orne noe ne eee 421
CHUNG. Dieu ey, : ©. Bente cure esac tet ae ee eet eee 11
TO PATRIPTO 2 AC 8 oP RO EO ONE ies a. fee ayes Seen ee es 190
DAVIES BAe Re: by oes ae, es RR En ae ree ee 278
DE REESE. (DSB eee fe cetera 1 a ee ee ee 40
ID SYN TVG 8 ON G Ga em nee Mee crs hha eta a! daly enic ole as 358
IBERNISSE IDE Mises 3:3 teas semeeecs oreeherc ede) ee eae ee 244
EGUOREA ID)! NAG e Sec n\ei-n hes ete tee Fee ape, ae Pee 342
FE MIER SONG) WV ere se see os aay ogee te ee ea 422
IESTINE Ts SY oon) hl cee g ye a ESE Lo Be econ eg eR 98
ROSTERS ING REA. ita gas Sete iene ch, vO ae rae 97, 98
GELEER PBS oases ce a ly ae ee 127
GITEMERSA RES Wi csi aa) Pom Ae a Ss ee 207
GOSTINERGSIM> Vike Arwen sy 2 ae eee 305, 315, 319
GREENWOOD SA 5G5 ae TAO ere eRe 90
(GUZIMANS SIGE SECS to, ote meren erent ne yiias pad Oyo even Ce 159
1s PNR AO} NEE] Us Gl genes arch srqss scab ols Sema a ara re mlo.s os culee 230
IEPARIASEWY.GH® MENG 4) Sep ernyceic a ee cae 76
ELARRINGTION, (Re Wis ccc cs.gitnee tee 2h RUEBEN: 148
EVASZPRIUINAREN (Geeks sens pene ree Senn ocean ee 196
TEAVINES At Fencing See Poa Rens GA ci ee 377
FED GPETH Jt Wis mee ied 8 eee wr RoI Re eee 1
PR RaZ Chae a =, Ss een, I St ae eee 190
FIO GK EY: JR SAWIRS ee, ce, 21a Bac eae ee 5
FLODGSON: AGING 256 ae ey ee ee eee 278
TEIOREMAN sspears en ee ee eee 96, 417
FOL YOAK WAS IRE cy ise wy eee re ee 369
FUG HES SIRS ING Ree 0. en eee ee Ae, Le ga a 422
AJONES ASRS al aoc eG a eT eater ze 267
KAN TORS SVIUIS ID ce 1.4.00 Heh, tes eo ig as mn eae 105
ISERSTIRGH EGA sy Seen A eugene pe Me eae ee 421
TWANWIRSVESES Vitek os, suits SEs dc ee 46

LES ROUX: Tos! GR oe as ae ce, er ee ee 400
LIB TVEDS W.JRe i. a ed Xe eee oe 400
LINDBERG DRG 2 oen seis 2 eee SOG eee ee 387
LiOPEZ5 Ancien 2 ic BE pe ea eee 295
LOPEZ): J 5 oo nhetes Seta oe ee Oe ee a eee 295
MARCHETTI, Ke By 2 ee en de eee 127
IMPARIDEYS Paral] ive rane OF 9 et nas ak rch 230
MIGICEAN: lJ RAG srs ae cree ets arc te ttee an cee 196, 408
INIONTOY:Aca VIB ar nr ey ee 2h Neh eee 295
MURRAVS AS 623.8) eres cee Oh Oe he 267
NEWMAN) IES i ete ad ioe ae estos Soy a 90
OSORIGHEL.. ii ie ee ts ie I 347
PAGE, Ali inerus ey a eet nee Rata oe 222
PARADASZES © 2 Ane cas ho oe eS eee 55
PEMBROKE WES Sere diac no ae onl eee 342
PERED OSs. oes ao ce OAR een eee oy eee ae 55
RETIRE ASS Pts aa Se eee 76, 424
PHIEETPS DS VWWisuces Aoi ads eats (103), (104), (332), (427)
PRABHAKAR AGRIAO NAYS. Ser ss a cea eso 173
IPRASADAVRIAO UW DNIG VEN Ae oO ee 173
RAMIREZ SINS Bias) Sei eget Oe 347
RIiOSsiG se Bis. Sieg eae. 0 eS 159
RO THAR Hee oe ens i tens Soe Sled NENG Eh 1 eee 95, 184
IRGVANE SPAIG Sass fre cit Duk SR Ut hos ao dom alc ae ee 5
SAIEAS 3 Ce ot Boon eid, bwie Bi chen et ee 421
SALGADOW iiss ere dene Stee Soe ee 347
SEGA WAMS icc iste lees be sys seas GRR Oe 230
SHIMEKAIRG Ses hs ao 1 eS ee 213
SIGNORMIRSEWEES 2 o6: 2G, ose ms cenene oe ee (212)
SINGHORS SMS kee 5 sstng aie ny ccs a eee ee 291
SKIBEBDERS Git Aue | 218. 3 v0 tacts enriere ae ee 267
SMOUSES D5, JR 0 65 os6.56 4.01555 Se eee 342
SO YER A) beets secep cose usie ye Saas al eRe eee eee 248
SPENCEMN Eis 2c.ohice2 5 np eS oe ea Ie ee eae 3)3)3}
SIPEBBING Sloe DS 5 xin case Wn ene ee Ra eae 95, 100
SYS O BVA OV ecgsyctis: i ichie 2 x dieu eh cae ee oar ca 105
SDERIWIEIGER JN (BS... ..< os ete ee 244
TRERWIEGIGERS (REC. 2. 534)54 See re See 244
THEO O MI QUIUNANIORS (Chacacascacacsvsdaavocancas 248
FISETONIPSON#G RSAC es eon Ta cee ee en 11
NAID VISA a8 5c css tices Te ee 173
WAL DEBENITO MWS. 55:6 aie Eee 55
WANS ERE SPORTS 2.5 cece yea eee rere ee ene ee 206
WATTATISW eZ. on OE ee 333
VIAN THE des Atos we ccs, 0 Feel nets cael eRe cal ee ee 134
VWAWINE: eA ene 2 Pe, cna ke eae ee 138
WBS Neo 2 8 che. on one ee Cee ee 69
AVVATITETEAIN 3 Real Chath Ah na os te eee 222
VV IETATAINAS = (Gan Cheetos a ne 315
AVIAING VV ac coy cas tarsile dene ats een 230

Page numbers for book reviews are indicated by parentheses.

iV

THE

VELIGER

A Quarterly published by

CALIFORNIA MALACOZOOLOGICAL SOCIETY, INC.
Berkeley, California

R. Stohler, Founding Editor

Volume 30

| a
401

V4x
MOLL

ISSN 0042-3211

July 1, 1987 Number 1

CONTENTS

In Memoriam: Sir Maurice Yonge, F.R.S. 1946; C.B.E. 1954; Kt. 1967.
SROEUMVEGELEDGEB UE ts eMas en uini atte all. Slr Nea Skala eee yells Vile aati eseeenes

pene ee NR
aA\TH SONIAn

variabilis by two species of Cinclodes (Aves: Furnariinae) in centr i 5 1997
Puitip A. R. HOCKEY, ALISON L. BOSMAN, AND PETER G. RYAN . §..... J UL | Nee

Seasonal growth patterns in the tropical littorinid snails Littorina angulifera,and LIBRARIED
Tectarius muricatus.

Jerr M. BuRGETT, JOHN D. CuBIT, AND RICARDO C. THOMPSON ....... 11

Courtship and dart shooting behavior of the land snail Helix aspersa.
ANNIE Ve) eet aC EDWIN Gade etnies 5 \-lcvenct yon (els epson istics sn jeve use eye. ee Mean 24

Ecology and burrowing behavior of Ascobulla ulla (Opisthobranchia: Ascoglossa).
DUP NINTS; Tip IONS, VETRTV OST, Ns, al ils a eigen) Hil ae te ee eRe OSs peer eA RIG Rela an Soa 40

Cryptomya californica (Conrad, 1837): observations on its habitat, behavior, anat-
omy, and physiology.
IEEE em EANWIR Wag ese Writ nen oe Sls hel maharey bis aaneiin Ritay tal Ma sienna ab ede a 46

Gametogenesis and reproductive cycle of the surf clam Mesodesma donacium
(Lamarck, 1818) (Bivalvia: Mesodesmatidae) at Queule Beach, southern
Chile.
SANTIAGO PEREDO, ESPERANZA PARADA, AND IVAN VALDEBENITO ........ 55

Oxygen uptake and the effect of feeding in Nautilus.
NAPE) PEE VESTED S Maen Mara ere MU MAE rete es ANUSUNOGIAL MeN che ilaigd RR) tins eur ia Ullal bela a 69

CONTENTS — Continued

The Veliger (ISSN 0042-3211) is published quarterly on the first day of July, October,
January and April. Rates for Volume 29 are $25.00 for affiliate members (includ-
ing domestic mailing charges) and $50.00 for libraries and nonmembers (including
domestic mailing charges). An additional $3.50 is required for all subscriptions sent
to foreign addresses, including Canada and Mexico. Further membership and sub-
scription information appears on the inside cover. The Veliger is published by the
California Malacozoological Society, Inc., % Department of Zoology, University of
California, Berkeley, CA 94720. Second Class postage paid at Berkeley, CA and
additional mailing offices. POSTMASTER: Send address changes to CEMES= Ince
P.O. Box 9977, Berkeley, CA 94709.

THE VELIGER

Scope of the journal
The Veliger is open to original papers pertaining to any problem concerned with mol-
lusks.

This is meant to make facilities available for publication of original articles from a
wide field of endeavor. Papers dealing with anatomical, cytological, distributional, eco-
logical, histological, morphological, physiological, taxonomic, etc., aspects of marine,
freshwater, or terrestrial mollusks from any region will be considered. Short articles
containing descriptions of new species or lesser taxa will be given preferential treatment
in the speed of publication provided that arrangements have been made by the author
for depositing the holotype with a recognized public Museum. Museum numbers of the
type specimen must be included in the manuscript. Type localities must be defined as
accurately as possible, with geographical longitudes and latitudes added.

Very short papers, generally not exceeding 500 words, will be published in a column
entitled “NOTES, INFORMATION & NEWS’; in this column will also appear notices
of meetings, as well as news items that are deemed of interest to our subscribers in
general.

Editor-in-Chief
David W. Phillips, 2410 Oakenshield Road, Davis, CA 95616, USA

Editorial Board

Hans Bertsch, National University, Inglewood, California

James T. Carlton, University of Oregon

Eugene V. Coan, Research Associate, California Academy of Sciences, San Francisco
J. Wyatt Durham, University of California, Berkeley

Terrence M. Gosliner, California Academy of Sciences, San Francisco
Cadet Hand, University of California, Berkeley

Carole S. Hickman, University of California, Berkeley

David R. Lindberg, University of California, Berkeley

James H. McLean, Los Angeles County Museum of Natural History
Frank A. Pitelka, University of California, Berkeley

Peter U. Rodda, California Academy of Sciences, San Francisco

Clyde F. E. Roper, National Museum of Natural History, Washington
Barry Roth, Santa Barbara Museum of Natural History

Judith Terry Smith, Stanford University

Ralph I. Smith, University of California, Berkeley

Wayne P. Sousa, University of California, Berkeley

T. E. Thompson, University of Bristol, England

Membership and Subscription
Affiliate membership in the California Malacozoological Society is open to persons (no
institutional memberships) interested in any aspect of malacology. As an affiliate member,
a person may subscribe to The Veliger for US $25.00, which now includes mailing
charges to domestic addresses. There is a one-time membership fee of US $2.00, after
payment of which, membership is maintained in good standing by the timely renewal of
the subscription; a reinstatement fee of US $3.00 will be required if membership renewals
do not reach the Society on or before April 1 preceding the start of the new Volume. If
a receipt is required, a self-addressed, stamped envelope (or in the case of foreign mem-
bers, the envelope and two International Postal Reply coupons) should be included with
the membership or subscription request.

The annual subscription rate to The Veliger for libraries and nonmembers is US
$50.00, which now includes mailing charges to domestic addresses.

An additional US $3.50 is required for all subscriptions sent to foreign addresses,
including Canada and Mexico.

Memberships and subscriptions are by Volume only (July 1 to April 1) and are payable
in advance to California Malacozoological Society, Inc. Single copies of an issue are US
$25.00 plus postage.

Send all business correspondence, including subscription orders, membership applications,
payments for them, changes of address, to: C.M.S., Inc., Post Office Box 9977, Berkeley,
CA 94709, USA.

Send manuscripts, proofs, books for review, and correspondence regarding editorial matters
to: Dr. David W. Phillips, Editor, 2410 Oakenshield Road, Davis, CA 95616, USA.

The Veliger 30(1):1-4 (July 1, 1987)

THE VELIGER
© CMS, Inc., 1987

In Memoriam: Sir Maurice Yonge,

F.R.S. 1946; C.B.E. 1954; Kt. 1967

An era of great achievement and distinguished contribu-
tions by English naturalists to the study of the seas came
to a close with the passing of C. M. Yonge (as he was
known for most of his long career) on 17 March 1986. He
was the last of the generation that included F. S. Russell,
Alister Hardy and George Deacon, and the best known
of all of them abroad. Our knowledge of the sea would be
less were it not for the work of these “Old Men of the
Sea,” and their students, and our library shelves would be
barren without their books and the symposia and serials
they edited.

Among Yonge’s most important contributions was his
work on mollusks, especially the functional morphology
of the bivalves. He began publishing on this subject with
a paper on feeding and digestion in Mya in 1923 and by
1974 he had published at least 170 papers, including 12
on Pacific coast mollusks; one of these appeared in The
Veliger (1962); most of the others were published in a
series of papers in the Uniwersity of California Publications
in Zoology and three in the Proceedings of the California
Academy of Sciences.

C. M. Yonge was born on 9 December 1899, about 14
months before the end of Queen Victoria’s reign. He was
named Charles Maurice (pronounced “Morris”), but he
never used the Charles. His father was Headmaster of
Silcoates School at Wakefield in Yorkshire, which he at-
tended, receiving a good basic education. While in school
he thought of becoming a journalist, but enlisted in the
army in 1917, too late, fortunately, to be sent to the trench-
es. When released from service after the war he went up
to Oxford with the intention of studying history, but after
a term decided on forestry and went to Edinburgh. There
he was exposed to zoology; entranced by his first dissection
(of a frog) he fell under the influence of J. H. Ashworth
(remembered for his studies of polychaetes) and from him
developed a life long fascination with marine invertebrates.
He was awarded the Baxter Natural History Scholarship
and began a study of digestion in Crustacea for his Ph.D.
An interlude at the Millport marine laboratory was his
introduction to marine biology. After completing his Ph.D.
he was employed as a physiologist at the Marine Biological
Station at Plymouth, where he studied digestion in oysters.
The pay was meager in those days and Maurice took to
writing popular articles for the newspapers to augment
his modest salary. In 1927 he teamed up with another
young staff member, FS. Russell, to write a popular book:

The Seas (Russell & Yonge, 1928). This book was an
immediate success, and was completely revised (essentially
a new book) by the authors in 1975. It is a monument to
the fine English tradition of scientific popularization, and
to a lifelong friendship as well. It may well be the only
book by two authors to survive almost 50 years and to be
rewritten by them. Many of us were confirmed in our
interest in the sea by reading this book in our youth and
in my own career it stands second only to 7wenty Thousand
Leagues under the Sea. It was an honor and privilege for
me to review the last edition of “Russell & Yonge”
(BiosScience, 1977). The book had an unexpected influ-
ence on Yonge’s career, for on the strength of his chapter
on coral reefs he was selected to be the director, at 28, of
an expedition to the Great Barrier Reef, sponsored at the
request of the Australian government by the British As-
sociation for the Advancement of Science while a Balfour
student at Cambridge. He had written the chapter more
or less by chance as it was one of several topics neither
author knew much about at the time. The decision was
not made on the toss of a coin, as rumor had it, however.
As it turned out, Maurice was an excellent choice as ex-
pedition head, managing even to return with a bit of change
left over from a very modest budget, although he remem-
bered that he made “every possible mistake.”

The Barrier Reef Expedition lasted over a year (from
the spring of 1928 to July of 1929), and was the first
expedition that investigated the general ecological aspects
of a coral reef and, thanks to Maurice’s skill as a writer,
resulted in his book A Year on the Great Barrier Reef (1930),
a classic of the literature of coral reefs. There was also a
splendid series of monographs. Most of the members of
the expedition had distinguished careers in the marine
sciences after the expedition. For Yonge it established his
reputation as an authority on coral reefs, his second spe-
ciality after the functional morphology of mollusks.

Maurice returned to Plymouth after the expedition, but
was soon called to Bristol as the first professor of zoology
there. During the war years he was the admirable Crich-
ton, living in the basement, meeting the needs of Kings
College, London, which had been evacuated from London,
serving as Dean of Science and firewatcher, among other
assignments. He was also awarded the George Medal.
Somehow he managed to keep up with his research, and
after the war (1944) was appointed Regius Professor at
Glasgow, where he spent the rest of his academic career.

Page 2 The Veliger, Vol. 30, No. 1

Figure 1

Sir Maurice Yonge giving an impromptu lecture at the University of Arizona’s field station at Puerto Penasco,
Sonora, 19 March 1972. Photographs on left, by John Hendrickson; photographs on right, by J. W. Hedgpeth.

In Memoriam: Sir Maurice Yonge, 1987

He presided over the largest zoology department in Great
Britain, became F.R.S. in 1946, and was much in demand
to serve on boards and commissions. For all of this he was
honored with the knighthood. He became a world traveller,
circling the globe so often for committee meetings in various
parts of the world, that he lost track of how many times
he had been around the world. Almost everywhere he went
he found some mollusk to study, and wrote it up. He
nevertheless accumulated quite a backlog and in his last
retirement years before his final illness, completed about
30 papers. Somehow, in all this he found the time to write
the great modern classic of seashore biology for the Collins
New Naturalist series (The Sea Shore, 1949) and to ac-
cumulate a splendid private library of books on the sea-
shore and mollusks. He also wrote a book on oysters for
the same series, and with T. E. Thompson, a book on
Living Marine Molluscs (reviewed by R. I. Smith in The
Veliger 20(2):187). His library included, among other rar-
ities, an obscure American item, a small work on con-
chology by Edgar Allan Poe. Fortunately this library has
been kept intact and is now at the university in Townsville,
appropriately near the Great Barrier Reef. It was my great
triumph to find under his nose in an Edinburgh bookstore
a small book he had never heard of, but reluctantly deferred
to his seniority and let him buy it.

In 1949 C. M. Yonge came to Berkeley as visiting pro-
fessor in the Department of Zoology for the spring term,
and for the summer course, held at Hopkins Marine Sta-
tion by arrangement with Stanford University. He was
being earnestly courted by the department at Berkeley to
replace S. F. Light, who had died in 1947. All sorts of
inducements and propositions were tried; he had fallen in
love with Pacific Grove and expressed the hope that an
arrangement might be made to work there, and President
Sproul was seriously considering arranging a joint pro-
fessorship with Stanford University. Maurice, however,
decided against leaving England, in part for his childrens’
sake. However, he returned to California several times,
and was a visiting professor at Friday Harbor and Seattle
for several occasions, and continued his observations of
mollusks on these trips; the Pacific Ocean appealed to him
more than the Atlantic and he found our mollusks “‘infi-
nitely fascinating.”

Yonge found his first experience with our educational
system a bit of a strain. Our custom of frequent in-session
examinations was something he had difficulty adjusting to,
and it is rumored that he threw one set of papers out of
the car window on the way to Berkeley. Ralph Smith, who
characterized himself as a “dour New Englander” was
also a new experience. In a letter to me during the session
at Pacific Grove, Maurice wrote that he had been working
very hard to live up to the expectations of that “‘austere
New England intellect.”

As a student of mollusks Yonge was a facile and accurate
observer of the living animals, and concentrated his atten-
tion on the action in the mantle cavity, as pointed out by

Page 3

Ralph Smith in the review cited above. The discovery of
Neopilina was to him an irrelevancy that really didn’t have
much to do with what interested him, as implied in his
commentary on the creature in Nature.* He was a good
lecturer, in spite of, or perhaps because of, his tendency
to stammer at times, and his treatment of that irrelevant
animal in an impromptu lecture at the University of Ar-
izona’s field station at Penasco, Sonora, in the spring of
1972 was probably typical. After drawing a sketch of Neo-
pilina on the blackboard, he contemplated it with some
disdain and got on to the bivalves as soon as possible, and
became more enthusiastic as he got more deeply into his
talk. The series of photographs, taken by myself and John
Hendrickson during this lecture, is a rare record of a
master at work (Figure 1).

At home Maurice was a popular professor, responsible
for many students who now hold significant posts in uni-
versities. Three students from California earned their Ph.D.
from him at Glasgow: Joseph H. Connell, Peter Fank-
boner, and Edmund H. Smith. Maurice was an affable,
easily approachable person (our friendship began with
correspondence about our libraries) whose first words to
me when I met him in the otherwise empty office once
inhabited by C. A. Kofoid was an apology for the racket:
“They’ve put me up here next to the doggery.”’ He listened
well and attentively, and if he had to disagree with you,
he did it pleasantly. He carried his many honors lightly
and lacked the well known tendency of some Britons (he
was born a Yorkshireman, but of a Dorset family) to be
a stuffed shirt. After his retirement from Glasgow he moved
to Edinburgh, the city of his student days, and became an
honorary member of the department there. Of the honors
ceremony for the knighthood in Edinburgh Castle he said:
“Too bad you weren’t here to see it. I was a sight to
behold!” I have Maurice to thank for many kindnesses,
not the least, perhaps, our expedition to find the grave of
Edward Forbes in a small cemetery in Edinburgh. We
almost missed it because the stone was covered with moss.
He assured me it would be cleaned up, and I am sure it
was. I need no stone to remember Maurice by.

Maurice considered that the seventies were the best years
of his life. On 18 October 1973 he was honored (with N.B.
Eales) for 50 years of publication by the Malacological
Society of London. He completed 30 papers during his
retirement, and characterized himself as “a straight zo-
ologist more and more fascinated by what evolution has
done with the bivalve form in the molluscs” (letter to
J.W.H., 17 Aug. 1976). He was active until his 83rd year,
when he developed Parkinson’s disease. His last years were
saddened by the steady attrition of life-long friends, and
at the last, by the death of his first son Robin from a fatal
heart attack in the Lagos airport. He is survived by his
second wife Phyllis (Lady Yonge), his daughter Elspeth,
his second son Christopher, and five grandchildren.

Joel W. Hedgpeth

Page 4

C. M. Yonge’s Papers on Pacific Coast Mollusks

1951.

1951.

LOSI.

1952.

1952.

1952.

Studies on Pacific coast mollusks. I. On the structure and
adaptations of Cryptomya californica (Conrad). Univ. Cal-
if., Publ. Zool. 55:395-400.

Studies on Pacific coast mollusks. II. Structure and ad-
aptations for rock boring in Platyodon cancellatus (Conrad).
Univ. Calif., Publ. Zool. 55:401—407.

Studies on Pacific coast mollusks. III. Observations on
Hinnites multirugosus (Gale). Univ. Calif., Publ. Zool. 55:
409-420.

Studies on Pacific coast mollusks. IV. Observations on
Suliqua patula Dixon and on evolution within the Soleni-
dae. Univ. Calif., Publ. Zool. 55:421-438.

Studies on Pacific coast mollusks. V. Structure and ad-
aptation in Entodesma saxicola (Baird) and Mytilimeria
nuttallu Conrad, with a discussion on evolution within the
family Lyonsiidae (Eulamellibranchia). Univ. Calif., Publ.
Zool. 55:439-450.

Studies on Pacific coast mollusks. VI. A note on Kellia

1953.

1958.

1960.

1960.

1962.

1962.

*11957.

The Veliger, Vol. 30, No. 1

laperousu (Deshayes). Univ. Calif., Publ. Zool. 55:451-
454.

Observations on Hipponix antiquatus (Linnaeus). Proc.
Calif. Acad. Sci. 28:1-24.

Observations in life on the pulmonate limpet 77imusculus
(Gadinia) reticulatus (Sowerby). Proc. Malacol. Soc. Lond.
33:31-37.

Mantle cavity, habits, and habitat in the blind limpet,
Lepeta concentrica Middendorff. Proc. Calif. Acad. Sci. 31:
103-110.

Further observations on Hipponix antiquatus with notes
on North Pacific pulmonate limpets. Proc. Calif. Acad.
Sci. 31:111-119.

On the biology of the mesogastropod T7ichotropis cancellata
Hinds, a benthic indicator species. Biol. Bull. 122:160-
181.

Ciliary currents in the mantle cavity of species of Acmaea.
Veliger 4:119-123.

Reflexions on the monoplacophoran, Neopilina galatheae
Lemche. Nature 179:672-673.]

Crest of the Yonges of Dorset.

“I am impressed by [your] coat of arms—but really not quite up

to mine....
to J.W.H. 17 Aug. 1976).

By permission from Fairbairn’s Crests,
© 1986 New Orchard Editions Ltd.

The Veliger 30(1):5-10 (July 1, 1987)

THE VELIGER
© CMS, Inc., 1987

The Maintenance of Polymorphism and Cryptic Mimesis

in the Limpet Scurria variabilis by ‘Two Species of

Cinclodes (Aves: Furnariinae) in Central Chile

PHILIP A. R. HOCKEY, ALISON L. BOSMAN, ano PETER G. RYAN

Percy FitzPatrick Institute of African Ornithology, University of Cape Town,
Rondebosch, South Africa 7700

Abstract. On the central Chilean coast, the intertidal limpet Scurrza variabilis is clinally polymorphic,
ranging from essentially non-cryptic individuals to individuals that are highly cryptically mimetic with
a barnacle model. Many species prey on S. variabilis, but birds, notably waders, such as oystercatchers,
and two species of C7nclodes are the only visual, selective predators present. The influence of Cinclodes
on limpet polymorphism is evidenced by the predominance of cryptic morphs in habitats accessible to
Cinclodes. Such differences in morph ratios between accessible and inaccessible habitats were not present
in areas without avian predators or where shorebirds, but not Cinclodes, were present. There is no
evidence of genetic influence by avian predators on local Scurria populations, although survival of
individual Scurria limpets is favored by polymorphism and particularly by cryptic mimesis. Selective
predation is considered to be the mechanism maintaining the polymorphism, but under present conditions
of predation, polymorphism is not considered necessary for survival of the Scurria population as a whole.

INTRODUCTION

Eucrypsis by virtue of homochromy and, to some extent,
active selection of specific substrata have been demonstrat-
ed to increase survival of Collisella limpets (Mollusca: Pa-
tellidae) in Pacific North America (GIESEL, 1970; MERCU-
R10 et al., 1985). Until recently the distribution of the genus
Collisella was thought to extend to Chile in Pacific South
America, with the limpet community of the mid-littoral of
the Chilean coast being dominated by one species, C. arau-
cana (d’Orbigny, 1839) (MARINCOVICH, 1973; CASTI-
LLA, 1976). The taxonomy of South American patellaceans
is poorly understood. Examination of specimens of “C.
* collected in central Chile in November 1985
shows that, on the basis of shell-structure characters and
plumbing of the heart vessels, these specimens belong to
the genus Scurria and are probably S. variabilis (Sowerby,
1839) (D. R. Lindberg, in litt.). The mid-littoral of central
Chile is characterized by extensive beds of small barnacles,
principally Chthamalus cirratus Darwin (CASTILLA, 1981),
and S. variabilis occurs both on bare rock surfaces and
among these barnacle beds. Scurria variabilis is clinally
polymorphic, ranging from individuals that are essentially
non-cryptic to individuals exhibiting extraordinary cryptic

araucana’

mimesis (sensu PASTEUR, 1982) due to homomorphy and
homochromy with the model C. czrratus (Figure 1). BOEHME
(1974) erroneously described the barnacle-like morph of
S. variabilis as a new species, Collisella boehmita.
Polymorphism in certain marine species has been shown
to be adaptive in reducing predator hunting success (e.g.,
HOAGLAND, 1977; REIMCHEN, 1979; PALMER, 1985). In
such instances it is reasonable to conclude that predation
pressure is a prime selective force in the evolution of poly-
morphism or mimicry in the prey species, although the
process by which a relative advantage accrues to divergent
phenotypes in the early stages of divergence has been dem-
onstrated on few occasions (BROWER ef al., 1971). Mimicry
in Scurria variabilis is visual and for any selective advantage
to accrue to mimetic individuals the predator(s) of S$. var-
iabilis must be assumed to forage both visually and selec-
tively. Intertidal predators in central Chile are numerous
and diverse, and many species have been studied in detail
(PAINE & PALMER, 1978; CASTILLA, 1981; BAHAMONDES
& CASTILLA, in press). The only predators present that
forage selectively using visual cues and prey on S. variabilis
are certain shorebirds (Aves: Charadriiformes) and two
species of Cinclodes (Aves: Furnariinae) (CASTILLA, 1981;

Page 6

The Veliger, Vol. 30, No. 1

Figure 1

The three recognized morphs of Scurria variabilis. Type 1 = non-cryptic; Type 2 = intermediate; Type 3 = cryptically

mimetic.

BAHAMONDES & CASTILLA, in press, and personal obser-
vations). This study quantifies the occurrence of poly-
morphism and mimicry in S. variabilis and identifies the
predators most likely to be responsible for maintaining
that polymorphism, based on predator occurrence and for-
aging behavior and on variations in morph ratios of S.
variabilis.

MATERIALS anp METHODS

Three morphs of Scurria variabilis were recognized: Type
1 exhibited no cryptic coloration or modification of shape;
Type 2 had a well-defined darker area apically, corre-
sponding approximately to the area occupied by the tergal
and scutal plates of a sessile barnacle; and, Type 3 was
cryptically mimetic, being in all respects, including the
outline of the tergum and scutum, an excellent mimic of
Chthamalus (Figure 1). The mimicry of Type 3 limpets
was So precise that on occasions it was necessary to remove
the animal from the rocks to determine whether it was a
limpet or a barnacle.

Absolute and relative frequencies of occurrence of the
three morphs were recorded at 17 sites in central Chile
between 30°S and 42°S during October and November
1985 (Figure 2). At each site, frequencies of occurrence
of the three Scurria morphs were recorded in the mid-
littoral using randomly positioned 10 x 10 cm quadrats

in two habitat types: (1) rocky slopes or flat areas accessible
to avian predators and (2) vertical or steep rock faces
inaccessible to avian predators. Between 8 and 76 quadrats
(0.08-0.76 m?) were sampled, dependent on limpet density.
Limpet densities per m* were calculated by simple ex-
trapolation from the area sampled at each site. Hence,
confidence limits are not presented.

The number of intertidal avian predators present per
100 m of shore at each site was assessed, and on this basis
three types of site were recognized: sites without avian
predators, sites with Cznclodes but with no (or very few)
shorebirds, and sites with many shorebirds but no Cin-
clodes.

RESULTS

At 13 of the 17 sites, less than 1% of all Scurria variabilis
were >12 mm in length (12 mm corresponding to the size
of a large specimen of Chthamalus cirratus). At sites Al-
garrobo 2 and 3, and at Ancud 1 and 2, up to 85% of all
S. variabilis were >12 mm in length.

At sites without avian predators there were (with one
exception) no significant within-site differences in the ra-
tios of the three Scurria morphs on rock faces accessible
and inaccessible to birds, but there was no consistency in
morph ratios among sites (Table 1). In addition, there
were no significant differences in the proportions of crypti-

Rar Aw RentlockeyacHialen LOST

cally mimetic (Type 3) morphs in the four habitats where
birds had no direct predatory impact viz.: accessible and
inaccessible habitats at sites without avian predators, and
inaccessible habitats at sites where either waders or Cin-
clodes were present (Kruskal-Wallis one-way ANOVA,
N, = 4, N, = 4, N;, = 4, N, = 9, HW = 5.51, P = 0.138).

At eight of the nine sites with Cinclodes present, there
was a significant difference in morph ratios between ac-
cessible and inaccessible rock faces. Non-cryptic (Type 1)
morphs formed a higher proportion of the Scurria popu-
lation on inaccessible than on accessible rock faces (mean =
35.2 SD of 21.7% vs. 17.3 16.2%) (Wilcoxon matched-
pairs signed-rank test, n = 9, 7 = 0.00, P= 0.008) and
the reverse was true of Type 3 morphs (38.1 + 16.9% vs.
52.9 + 19.4%;n =9, T = 1.00, P= 0.011). Type 2 morphs
were slightly better represented in accessible (* = 29.8 +
14.3%) than in inaccessible (¥ = 26.7 + 12.5%) habitats,
but the difference was not significant (n = 9, T = 9.00,
P =0.110). In addition, the site with the highest density of
Cinclodes (viz. Los Molles 1) showed the greatest difference
between morph ratios in accessible and inaccessible sites,
with the limpet population on accessible rocks being strongly
biased towards mimetic individuals (Table 1, Figure 3).

Densities of foraging shorebirds were much higher than
those of Cinclodes (up to 200 birds per 100 m of shore)
but, at sites where shorebirds were present, the proportions
of non-cryptic (Type 1) and mimetic (Type 3) Scurra in
accessible and inaccessible habitats were not significantly
different (Wilcoxon matched-pairs signed-rank test: Type
1,n = 4, 7 = 0.00, P = 0.068; Type 3, n = 4, T = 3.00,
P = 0.465).

DISCUSSION

True mimicry in limpets is rare. There is a morph of the
Pacific Collisella stanfordiana that resembles the toxic on-
chidiid Hoffmanola hansi (YENSEN, 1973), an example of
Batesian mimicry. There is a barnacle-imitating morph of
the Australian Patelloida latistrigata (G. M. Branch, per-
sonal communication) and in the Gulf of California, Col-
lisella acutapex resembles the barnacle Balanus amphitrite
(YENSEN, 1973). The adaptive advantage of these mimics
has not been investigated. Scurrza variabilis exhibits clinal
polymorphism, with an extreme morph showing cryptic
mimicry of Chthamalus barnacles.

On the central Chilean coast there are several vertebrate
and invertebrate predators of limpets (reviewed by CASsTI-
LLA, 1981), but most of these have been shown to remove
both limpets and barnacles using tactile stimuli in a non-
selective manner. Examples of such predators are the sea-
star Heliaster helianthus (Lamarck, 1816), the muricid
Concholepas concholepas (Bruguiére, 1789) (CASTILLA et
al., 1979; CASTILLA, 1981) and the suckerfish Sicyaces san-
guineus Muller & Troschel (PAINE & PALMER, 1978;
CASTILLA, 1981). Small numbers of Scurria variabilis have
been found in the gut of the surfbird Aphriza virgata (Gme-
lin, 1789), possibly ingested coincidentally when feeding

Oo (e)
W 72 W

'

’
‘
\
!

Totoralillo» Coquimbo

!

)
alparaifso

Algarrob a
g eSantiago

Las Salinas®
Punta EI Lacho

42S
Chiloé Island

Figure 2

Map of the study area.

on its preferred prey, the mussel Semimytilus algosus (R.
Navarro, personal communication). The Kelp Gull Larus
dominicanus preys on intertidal limpets, but Scurria vari-
abilis is not an important prey species, the larger eulittoral

Page 8

The Veliger, Vol. 30, No. 1

Table 1

Morph ratios and densities of Scurria variabilis, and densities of Cinclodes spp. at 17 sites in central Chile, October-
November 1985.

; Cin-
Scurria
density /m? Goges
Site type CSS /
Study site Acc. Inacc.* 100m _ Sp.f 1
No avian predators
Totoralillo 1 183 263 0.0 31
Los Molles 3 684 804 0.0 69
Los Molles 4 1141 1100 0.0 19
Los Molles 5 950 3725 0.0 19
+ Cinclodes
Totoralillo 2 635 460 1.0 nl 1
Los Molles 1 2770 418 6.0 ni 2,
Los Molles 2 low low 1.3 ni 43
Algarrobo 1 628 (e5y); 0.2 ni 38
Punta El] Lacho 2153 1205 1.0 nl 28
Mehuin 1 464 374 1.0 pa 6
Mehuin 2 760 527 0.6 pa 1
Ancud 1 244 179 1.0 pa 19
Ancud 2 543 Qi 1.0 pa 18
+Shorebirds
Algarrobo 2 318 79 0.0 45
Algarrobo 3 952 low 0.0 45
Las Salinas 1 703 610 0.0 40
Las Salinas 2 1133 893 0.0 35

* Acc. = Accessible, Inacc. = Inaccessible.
f ni = Cinclodes nigrofumosus, pa = Cinclodes patagonicus.

Accessible habitat
Morph type (%)

2

Inaccessible habitat
Morph type (%)

3 ON ih OR nN x P
54 139 AQ Al 49 137 DAD n.s.
1G 7 yy if 26 20 <2, <0.05e
60 194 IG 13 Tl 76 4.98 n.s.
49 190 16 41 43 298 3.03 ns.
59 165 15 30 55 138 18.85 <0.001
1 Dy 6 18 29 ny 85.21 <0.001
50 129 16 3 BB WM 53 <O0.001
113 Q 16 2B i106 DEG <OMi
DO) 303 5] 8D OR De 8.01 <0.05
66 116 ID Bl. SO AS 8.77. <0.05
77 152 OF 26 65) 158 11.53 <0.01
48 122 Mm Wi 25. 125 5.93 n.s.
36 190 2 4 2 95 9.47 <0.01
22. 159 69 17 14 35 6.99 <0.01
14. 238 OG 7 19 47 9.70 <0.01
31. 207 AB Bl WS 4.35 n.s.
22 345 46 26 28 268 18.28 <0.001

+ At this site there were more cryptic limpets on inaccessible slopes, an opposite trend to that found elsewhere. This is indicated by

a negative x? value.

Collisella zebrina being taken preferentially (BAHAMONDES
& CASTILLA, in press). The marine otter Lutra felina (Mol-
ina, 1782) occurs commonly on exposed coasts in central
Chile, but its intertidal feeding activity is confined to the
eulittoral zone and Scurria variabilis is not recorded as a
prey item (CASTILLA & BAHAMONDES, 1979). The extent
of predation by fish other than Sicyaces sanguineus during
the high tide period is unknown, but few, if any, species
other than Stcyaces sanguineus are likely to possess the
morphological adaptations necessary to remove limpets from
rock faces.

Based on the above, we hypothesized that the predators
most likely to be morph-specific in their predation of Scur-
ria variabilis were the Blackish Oystercatcher, Haematopus
ater Vieillot & Ondart, 1825, which is recorded as preying
on S. variabilis (CASTILLA, 1981), and two species of Cin-
clodes, an avian genus endemic to South America (HOWARD
& Moore, 1980). The Seaside Cinclodes C. nigrofumosus
(@Orbigny & Lafresnaye, 1838) and the Duskybellied
Cinclodes C. patagonicus (Lesson, 1828) both occur on the
coast of central Chile, although the former does not occur
south of about 39°S (JOHNSON & GOODALL, 1967). Cin-
clodes migrofumosus is exclusively coastal, whereas C. pa-
tagonicus occupies a range of habitats: both species include

mid-intertidal barnacle beds within their range of foraging
habitats and prey on S. variabilis (personal observations).
Haematopus ater was observed at Algarrobo and Los Molles
2, but not at other sites. Effects of predation on S. varzabilis
by this species are likely to be inseparable from the effects
of Cinclodes.

In areas where Cinclodes spp. are present, differences
in morph ratios between accessible and inaccessible hab-
itats provide clear evidence for the selection of non-cryptic
morphs by Cinclodes. At high Cinclodes densities, the bias
towards mimetic morphs in the limpet population is more
pronounced (Table 1, Figure 3). Shorebirds, even though
they occur at much higher densities than Cinclodes in some
areas, have a negligible impact on Scurrza morph ratios as
evidenced by insignificant differences in morph ratios be-
tween accessible and inaccessible microhabitats (Table 1).
This may be due to the concentration of their feeding
activity in the low- rather than mid-shore region (personal
observations). Some wader species may not prey on Scurria
at all, and the nocturnal feeding habits of some species
(movement rather than coloration of the prey probably
being the prime visual cue to predators at night) would
not result in morph-specific predation.

The impact exerted by visual, selective predators, chiefly

IP, Ae IR, IBlOOKay Ge Gilles, INST

Page 9

100

0 10 20 30 40 50 60 70 80 90 100 0 10 20 30 40 50 60 70 80 90 100 0 10 20 30 40 50 60 70 80 90 100
TYPE 1 TYPE 1 TYPE 1
Figure 3

Ternary diagrams illustrating the relationship between morph ratios of Scurria and predation. A, no avian predators;
B, with Cinclodes; C, with waders. Lines join crosses (accessible microhabitats) to solid circles (inaccessible micro-
habitats) at the same site. The larger crosses and dots in Figure 3B refer to sites at which the density of Cinclodes

was >1 bird per 100 m of shore.

Cinclodes, on the survival of different morphs of Collisella
is striking, but localized to the extent that morph ratios
on inaccessible slopes within Cinclodes territories and in
wader feeding areas do not differ from one another or from
the morph ratios in areas where there are neither Cinclodes
nor waders present. These observations suggest that, al-
though Cinclodes may have a local influence on the occur-
rence of phenotypes, these birds are not exerting a de-
tectable local genetic influence on the population, nor is
limpet density correlated with predator abundance (Table
1). The presumed pelagic larval stage of Scurria limpets
would tend to confound anything other than major local
genetic influences. A situation exists on the central Chilean
coast in which the predator apparently exerting the major
influence on Scurria phenotypes in central Chile occurs
patchily and at low density and appears to have no influ-
ence on Scurria density. At the same time, S. variabilis shows
an effective and highly elaborate polymorphism that has
arisen in the apparent absence of any strong selective force
that is still evident today. However, despite the fact that
predatory pressure is low, the selectivity of the predator
provides the mechanism for the maintenance of polymor-
phism in the prey, inasmuch as the incipient mimic (sensu
BROWER et al., 1971), the Type 2 Scurria, enjoys a selective
advantage over the non-cryptic Type 1 individuals. The
absolute abundance of Type 1 morphs suggests that, under
present predation pressures, polymorphism is not essential
for the survival of the S. variabilis population as a whole
but strongly favors the survival of cryptically mimetic in-
dividuals in the presence of predatory Cinclodes.

ACKNOWLEDGMENTS

We are grateful to Professor Juan Carlos Castilla of the
Pontificia Universidad Catolica de Chile and to Professor
Carlos Moreno of the Universidad Austral de Chile for
the use of field station facilities on the Chilean coast and

for logistical help. Professor George Branch, Dr. Fabian
Jaksic and an anonymous referee are thanked for helpful
comments on an earlier draft. We thank Dr. David Lind-
berg for identifying the Chilean limpet specimens. This
paper forms part of the FitzPatrick Institute’s 25th an-
niversary expedition to Chile. This work was supported
financially by the South African CSIR and the University
of Cape Town.

LITERATURE CITED

BAHAMONDES, I. & J. C. CasTILLa. In press. Predation of
marine invertebrates by the Kelp Gull Larus dominicanus in
an undisturbed intertidal rocky shore of southern Chile.
Revista Chilena de Historia Natural.

BOEHME, J. R. 1974. Nuevas especies chilenas de Lucabina,
Fissurella y Collisella (Mollusca, Archaeogastropoda). Bol.
Mus. Hist. Natur. Chile 33:15-34.

BRowER, L. P., J. ALCOcK & J. V. Z. BROWER. 1971. Avian
feeding behaviour and the selective advantage of incipient
mimicry. Pp. 261-274. Jn: R. Creed (ed.), Ecological genetics
and evolution. Oxford: Blackwell.

CasTILLA, J. C. 1976. Guia para la observacion del litoral.
Santiago: Editora Nacional Gabriela Mistral.

CASTILLA, J. C. 1981. Perspectivas de investigacion en estruc-
tura y dinamica de comunidades intermareales rocosas de
Chile central. II. Depredadores de alto nivel trofico. Medio
Ambiente 5:190-215.

CASTILLA, J. C. & I. BAHAMONDES. 1979. Observaciones con-
ductuales y ecologicas sobre Lutra felina (Molina) 1782 (Car-
nivora: Mustelidae) en las zonas Central y Centro-Norte de
Chile. Arch. Biol. Med. Exper. 12:119-132.

CASTILLA, J. C., C. GuisaDo & J. CANCcINO. 1979. Aspectos
ecologicos y conductuales relacionados con la alimentacion
de Concholepas concholepas (Mollusca: Gastropoda: Murici-
dae). Biologia Pesquera Chile 12:99-144.

GIESEL, J. T. 1970. On the maintenance of a shell pattern and
behaviour polymorphism in Acmaea digitalis, a limpet. Evo-
lution 24:98-119.

HOAGLAND, K. E. 1977. A gastropod colour polymorphism:

Page 10

one adaptive strategy of phenotypic variation. Biol. Bull.
152:360-372.

Howarp, R. & A. Moore. 1980. A complete checklist of the
birds of the world. Oxford: Oxford University Press.
Jounson, A. W. & J. D. GooDALL. 1967. The birds of Chile,

Vol. II. Buenos Aires: Platt Establecimientos Graficos S.A.

MarINcovicH, L., JR. 1973. Intertidal mollusks of Iquique,
Chile. Bull. Natur. Hist. Mus. Los Angeles County 16:1-
49.

MeErcuRIO, K.S., A. R. PALMER & R. B. LOWELL. 1985. Pred-
ator-mediated microhabitat partitioning by two species of
visually cryptic, intertidal limpets. Ecology 66:1417-1425.

PaINnE, R. T. & A. R. PALMER. 1978. Sicyases sanguineus: a

The Veliger, Vol. 30, No. 1

unique trophic generalist from the Chilean intertidal zone.
Copeia 1978(1):75-81.

PALMER, A. R. 1985. Adaptive value of shell variation in Thais
lamellosa: effect of thick shells on vulnerability to and pref-
erence by crabs. Veliger 27:349-356.

PASTEUR, G. 1982. A classificatory review of mimicry systems.
Ann. Rev. Ecol. Syst. 13:169-199.

REIMCHEN, T. E. 1979. Substratum heterogeneity, crypsis and
colour polymorphism in an intertidal snail (Littorina mariae).
Can. Jour. Zool. 57:1070-1085.

YENSEN, N. P. 1973. The limpets of the Gulf of California
(Patellidae, Acmaeidae). M.S. Thesis, University of Arizona,
Tucson. 146 pp.

The Veliger 30(1):11-23 (July 1, 1987)

THE VELIGER
© CMS, Inc., 1987

Seasonal Growth Patterns in the Tropical Littorinid

Snails Littorina angulifera and Tectarius muricatus

by

JEFF M. BURGETT,' JOHN D. CUBIT,? anp RICARDO C. THOMPSON

Smithsonian Tropical Research Institute, Apartado 2072,
Balboa, Republic of Panama

Abstract.

The seasonality of growth rates in the supralittoral snails Littorina angulifera and Tectarius

muricatus was investigated from 1978 to 1983 at Punta Galeta, on the Caribbean coast of Panama.
Growth rates were determined from individually marked animals that were measured at monthly
intervals. Meteorological and hydrographic conditions were monitored concurrently. Although the cli-
mate at this site was strongly seasonal, the growth rates of L. angulifera between 7 and 15 mm in length
showed no seasonal pattern. Growth rates of L. angulifera larger than 15 mm peaked during the local
dry season. Individuals of 7ectarius muricatus less than 15 mm in length were too rare in the study area
for examination of seasonal growth rates, but the growth of larger individuals was highest in the wet
season. For both species, growth rates of individuals less than 15 mm in length decreased linearly with
increasing size. Growth in larger individuals of both species occurred in discrete episodes separated by
variable periods without growth. Maximum growth rates of both species were about five times faster

than those previously reported.

INTRODUCTION

Galeta Reef, Panama, is in the southernmost region of the
Caribbean Sea, less than 10° north of the equator. Despite
the low latitude, however, growth rates, abundances, and
reproductive patterns of organisms in the subtidal and
lower intertidal habitats of this reef vary seasonally, ap-
parently in response to annual fluctuations in atmospheric
and sea conditions (HENDLER, 1977; HAy & Norris, 1984;
CusirT et al., 1986; Connor, Cubit, Hay, Kilar, Norris,
unpublished data). Terrestrial organisms in nearby hab-
itats also show strong patterns of seasonality in various
aspects of their biology (references in LEIGH et al., 1982).
Here we describe seasonality in the growth rates of two
species of littorinid snails that occupy the ecotone between
the marine and the terrestrial environments on the Carib-
bean coast of Panama.

Herbivorous gastropods are the predominant animals at
the highest levels of many shores throughout the world
(UNDERWOOD, 1979). Most studies of their growth have
been in temperate and subtropical areas, where fluctua-
tions in growth rates are associated with the winter—sum-

' Present address: Department of Zoology, University of Ha-
wall, Honolulu, Hawaii 96822, U.S.A.
* Please send reprint requests to this author.

mer seasonality of higher latitudes (FRANK, 1965a;
SUTHERLAND, 1970; NicotTri, 1974; BoRKowsKI, 1974;
McQualp, 1981; PHILLIPS, 1981). Relatively few gastro-
pods have been examined for seasonal patterns of growth
in the tropics, where seasonality involves a much different
combination of weather factors (FRANK, 1969; LEwIs et
al., 1969; YAMAGUCHI, 1977). Only a few of these tropical
studies involved snails of the upper intertidal zones (LEWIS
et al., 1969).

The littorinid snails monitored for growth in this study
were found in the supralittoral zones of two adjacent, but
much different, habitats: mangrove trees and rocky shore.
Concurrent monitoring of several physical variables de-
fined some aspects of local seasonality, and our analysis
was designed to assess the degree to which snail growth
reflected these environmental changes. This study was ini-
tiated by J. Cubit and R. Thompson and the data were
analyzed by J. Burgett.

Study Species

Littorina angulifera Lamarck, 1822, is found on both
sides of the tropical Atlantic, and may be synonymous with
L. scabra (Linnaeus, 1758) of the Indo-Pacific (ROSEWA-
TER, 1970). Although in protected waters it may occur on
smooth artificial surfaces, L. angulifera is most commonly

Page 12

found on the red mangrove Rhizophora mangle Lamarck,
1753 (PLAZIAT, 1984). Individuals less than 10 mm in
shell length are restricted to within a few centimetres of
the waterline, but larger snails range to all levels of the
mangrove trees (LENDERKING, 1954). The snails can be
observed apparently feeding on the surfaces of leaves and
stems, but most grazing probably occurs during nocturnal
migrations to the lower levels of the prop roots (P. Gu-
tierrez, unpublished data). Fragments of diatoms and cy-
anobacteria can be found in the fecal pellets (J. Burgett,
personal observations). Littorina angulvfera cements itself
to the undersides of stems and leaves and remains retracted
during most daylight hours (J. Burgett & R. Thompson,
personal observations).

Tectarius muricatus (Linnaeus, 1758) occurs higher on
the rocky shores of the Caribbean than other gastropods
(BANDEL, 1974). It can remain immobile and retracted
into the shell for long periods, adhering to the surface with
a spot of mucus. Tectarius muricatus grazes at night or
during heavily overcast days (J. Burgett, personal obser-
vations). Fragments of cyanobacteria and siliceous and
carbonate rock can be found in the fecal pellets (J. Burgett,
personal observations), suggesting a diet of epilithic and
endolithic algae and cyanobacteria similar to that of T.
grandinatus (Gmelin, 1791) in Polynesia (SALVAT &
DENIZOT, 1982).

MATERIALS anp METHODS
Study Areas

Study areas were on the fringing reef at Punta Galeta,
on the Caribbean coast of Panama (9°24'18’N,
79°51'48.5”"W), adjacent to the Galeta Marine Laboratory
of the Smithsonian Tropical Research Institute. The to-
pography and development (MACINTYRE & GLYNN, 1976)
and invertebrate fauna (CUBIT & WILLIAMS, 1983) of this
reef have been described elsewhere.

Littorina angulifera was studied on two adjacent clumps
of Rhizophora mangle rooted in a sandy area at the back
of the reef flat. No other gastropods were observed above
water level on these trees. The two clumps lacked prop-
root connections to the neighboring forest and were chosen
for this study to minimize dispersal of marked snails from
the study area. Growth of the clumps during the study
was estimated using aerial photographs taken in 1973,
1980, and 1984. By interpolation, the roots covered 8.5 m?
in 1978 and grew to cover 16 m? by the end of the study
in 1983. The tree crowns in 1984 were 2.8 and 3.7 m
above the elevation of the sand bottom, which was between
—2 and +6 cm relative to Mean Low Water (MLW, see
Environmental Monitoring below).

The study area for Tectarius muricatus was a wall made
of coral blocks and concrete mortar bordering the back-
reef, approximately 5 m from the Littorina angulifera study
area. The wall, approximately 30 years old, was 0.7 m
high and 16.5 m long, with a base in sand and coral rubble

ihe Welicers Volas0 Nom

27 to 35 cm above MLW. Two smaller species, Nodilit-
torina (Littorina) interrupta (Morch, 1876) and N. (L.)
angustior (C. B. Adams in Philippi, 1847) (nomenclature
after BANDEL & KADOLSky, 1982), occurred on the lower
parts of the wall.

Sampling and Marking

All Littorina angulifera found on the trees were collected
and marked between 19 September 1978 and 5 March
1982. After the latter date no new snails were collected,
and the L. angulifera study was ended in March 1983.

The cryptic habit of the snails and the structural com-
plexity of the trees made total collections difficult; there-
fore, estimates of recruitment were inexact. Because of the
ability of Littorina angulifera to disperse by floating (J.
Cubit & R. Thompson, personal observations) and the
reappearance of individuals missing for up to eleven months,
disappearance of snails could not be regarded as mortality.

Only a subset of the Tectarius muricatus on the wall was
monitored during the study, which ran from July 1978 to
April 1983. Small individuals of 7. muricatus were rare
in the study area, a situation also found at other sites
(LEwIs et al., 1969; BORKOWSKI, 1974). All marked snails
visible on the wall were collected for each sample. If fewer
than 50 marked animals were recovered, unmarked in-
dividuals were added to the study to make up this number.
Recruitment, density, and mortality were not estimated.

Snails were kept for less than 24 h in wet containers in
the laboratory while being measured and marked. The
length of each shell (7.e., height or longest dimension) was
measured with vernier calipers to the nearest 0.1 mm.
Growth was determined from extension of the shell margin
or lip, which was a more sensitive measure than increase
in overall length (LARGEN, 1967). A line of quick-drying
enamel (Nissen Metal Marker) was applied to the outer
surface of the shell margin after length measurement. At
the next collection, the maximum growth past this line
was measured to the nearest 0.05 mm using a dissecting
microscope fitted with an ocular micrometer. The previous
lip marking was then removed and a new line applied.
Individuals were identified by numbered plastic bee tags
(BERTNESS, 1982) attached with cyanoacrylate glue (Lit-
torina angulifera) or by hand-painted numerals (Tectarius
muricatus). After processing, the snails were taken to the
study areas and allowed to adhere to the substratum before
release.

Growth Analysis

Analyses of growth measurements from each sample
were limited to snails also collected in the immediately
preceding sample, so that the growth rates from each sam-
ple were based on a constant interval. Growth was con-
verted to daily rates by dividing the measured lip extension
of each snail by the number of days in the sample interval,
which ranged from 28 to 50 days. This growth rate was

J. M. Burgett e¢ al., 1987

assigned to the arithmetic average of the snail’s lengths at
the beginning and end of the interval (GULLAND & HOLT,
1959; VAN DEVENDER, 1978).

A regression-based model of growth could not be applied
to the entire length range of Littorina angulifera because
of differences in the length-growth rate relationships of
small and large snails. Growth rate variances could not be
normalized owing to the predominance of zero values at
some lengths (SOKAL & ROHLF, 1981:460). Moreover, the
discontinuous growth patterns of the larger snails were
not consistent with a continuous function (LOCKWOOD,
1974). Regression techniques were appropriate for small-
er, continuously growing animals. Because virtually all
snails smaller than 14 mm grew between samples, we
divided the data sets at this length and analyzed data from
the two size classes separately. The larger size class (> 14
mm) unavoidably contained both snails that had not stopped
growing and those that had resumed growth.

We restricted our regression analyses of the smaller size
class (<14 mm) to the 26 samples that contained at least
10 small animals. In all of these samples, preliminary tests
showed significant (P < 0.05) product-moment correla-
tions between length and growth rate. The functional re-
lationships between length and growth rate were deter-
mined for each sample using the geometric mean (GM)
method for Model II linear regressions (RICKER, 1973).
To facilitate the corrections detailed below, these regres-
sions were done using the rates of length increase rather
than lip extension.

Because growth was a decreasing function of length, and
the data were length differences over finite intervals rather
than instantaneous rates, the true growth rates of the snails
were underestimated (KAUFMANN, 1981; SUNDBERG, 1984).
Use of average length rather than initial length on the
abscissa reduced this error (LOCKWOOD, 1974), which was
a function of the growth rate and the length of the sample
interval (YAMAGUCHI, 1975; SUNDBERG, 1984). The error
was negligible at low growth rates and zero at the x-in-
tercept.

The slopes obtained by GM regression were corrected
for this error by the following procedure. For each sample
an arbitrary regression of growth rate on length was con-
structed with the same x-intercept as the GM regression.
Starting from several initial lengths, daily growth incre-
ments were calculated from this slope for the number of
days in the sample interval. The slope was adjusted until
the growth rates and average lengths obtained at the end
of the simulation fell on the GM regression line calculated
from the observed data. The absolute values of these cor-
rected slopes yielded the von Bertalanffy growth coefficient,
K, with higher values of K representing faster growth rates
at all sizes smaller than the x-intercept. The 95% confi-
dence intervals of the original GM regressions (RICKER,
1973) were used with the corrected slopes.

The frequency distributions of growth rates for the larg-
er Littorina angulifera were not consistently fit by normal,

Page 13

log-normal, or delta distributions (PENNINGTON, 1983).
The growth rates of this size class and of Tectartus muri-
catus were therefore summarized by the sample medians.

Environmental Monitoring

As part of a continuing monitoring program, water level,
air temperature, salinity, rainfall, wind speed, and wind
direction were measured for the duration of the study.

Water level over the central reef flat was recorded on a
continuous chart by a Stevens Type-A water-level recorder
mounted in a stilling well. Water levels were read from
the charts using a digitizer. CUBIT et al. (1986) present
details of this method and a discussion of the water-level
regime at Galeta. Water levels and elevations of the study
areas are expressed with reference to the 10-yr MLW
described in that paper. The average daily tidal range was
24.5 cm (CUBIT et al., 1986).

Rain from a rooftop collector was recorded by another
Stevens recorder. Data were digitized from the charts and
combined into weekly totals.

Daily maximum and minimum air temperatures were
read five mornings per week from a recording thermometer
originally suspended beneath the laboratory dock. In Jan-
uary 1981 the thermometer was moved to a shaded, ven-
tilated enclosure of polystyrene foam. Sea surface salinity
was measured five mornings per week using a hand-held
refractometer.

Wind speed and direction were recorded on a continuous
chart by a mechanical weather station (Meteorology Re-
search, Inc., model 1072) and converted to numeric values
by hand. The daily mean speed of winds from the northern
quadrant was cubed to yield a value proportional to north-
erly wind energy. This measure was assumed to be cor-
related with the intensity of wind-driven waves as well as
with other effects of wind, such as transport of salt spray.
Waves driven by northerly winds are suspected to raise
water levels on the Galeta reef flat (CUBIT et al., 1986),
and can reach the back-reef areas when water levels are
high. Swells from distant sources could not be estimated
from local data.

Daily values of total radiant exposure, or insolation
(wavelengths 280-2800 nm), were recorded from an Epp-
ley pyranometer at the U.S. Army Tropic Test Center’s
open sunfield at Fort Sherman, a coastal site 11 km from
Galeta.

Instrument failures resulted in incomplete data sets for
all variables except rainfall. Only weeks containing four
or more days of data were used to calculate weekly means
for the other variables. Four-week running averages were
computed from the weekly values using a minimum of
three weeks of data per four week period.

The unbroken time series for rainfall was used as the
representative seasonal variable in tests for correlation with
snail growth rates. Growth rates were also tested for cor-
relation with maximum water level because of its less

Page 14 The Veliger, Vol. 30, No. 1

(km/hr)? x 10° ppt °C

cal/ cm? / day

cm/ we

cm above MLW

43 a Max. Water Level

EN a cae ee

Air Temp.

rately elm iy 7 None Drmreg tet D Ponptrred Ph

yrs nT
ALA. a

Solar een ; }

|
:
e

T.m.
Se Se tt tt tt ttt
Jul Jan Jul Jan Jul Jan Jul Jan Jul Jan
1979 1980 1981 1982 1983
Figure 1

Environmental variation and sampling periods during the study. Light lines are weekly totals (rainfall) or weekly
means of daily values (all others); heavy lines are running means of weekly values for previous four weeks. Variables:
a, maximum water level above Mean Low Water; b, maximum and minimum air temperature; c, surface salinity;
d, wind from northern quadrant (NE-NW)); e, total radiant exposure (280-2800 nm); f, rainfall; g, sampling
schedule for L. angulifera (L.a.) and T. muricatus (T.m.). Samples used in analysis of growth (vertical marks) are

separated by solid lines showing length of sample intervals. Measurements after sample intervals longer than 50
days (dotted lines) were not used.

JME Burgett ec al. 1987

seasonal character and its potential importance to these
supralittoral snails. In these correlations, median growth
rates were paired with the running means of the physical
variables from the previous four weeks.

RESULTS

Environmental Seasonality

The dry season at Galeta usually began in December
and ended in May or late April, and was characterized by
strong northerly trade winds, high maximum water levels,
high insolation, little rain, and salinity over 33%c (Figure
1). The wet season made up the remainder of each year,
with more rainfall, lighter winds, less insolation, and lower
salinity. A short period of dry season weather usually
interrupted the wet season between August and October.
Although the maximum air temperatures were generally
higher from May to September, minimum temperatures
were relatively stable. Rainfall was anomalously low in
1982, possibly owing to the strong El Nino phenomenon
of that year. The consistent nature of the annual cycle was
reflected in the high correlations between most of the phys-
ical variables (Table 1). Gaps in the sampling schedule of
the snails (Figure 1g) occurred principally near the tran-
sitions between dry and wet seasons.

Water levels on the Galeta reef flat are affected by the
combined action of waves, tidal patterns, and fluctuations
in mean sea level (CUBIT ef al., 1986). Maximum water
level had lower correlation with the other factors (Table
1) because its period was approximately double that of the
main seasonal cycle. Peaks in this variable (Figure 1a)
occurred in both the dry and wet seasons, with a low point
after the dry-to-wet season transition. The maximum water
levels were rarely below the bases of the mangrove roots
(—2 to +6 cm relative to MLW), but the base of the
Tectarius muricatus study area (+27 cm) was above the
high water line for several weeks at a time, usually between
April and July.

Growth of Littorina angulifera

Selected scatterplots of growth rate versus length (Fig-
ures 2a-c) illustrate several features of growth in Littorina
angulifera examined in more detail below. Growth rates
were fastest in the smallest animals, and showed a roughly
linear decline with length up to about 15 mm. At lengths
over 14 mm, a variable proportion of snails showed no
growth during the sample intervals. The maximum growth
rate and the rate at which growth decreased with size
varied over time.

As explained above, data from Littorina angulifera 14
mm long and smaller were analyzed separately from the
data for larger snails. The growth coefficient of the smaller
size class was computed by regression analysis of change
in length, rather than the lip extension used to measure
growth in larger L. angulifera. The close, linear relation-

Page 15

Lip Growth/ day (mm)

Lip Growth/ day (mm)

Lip Growth/ day (mm)

6 10 14 18 22 26
Average Shell Length (mm)

Figure 2

Littorina angulifera. Growth rate versus average of shell length
at start and end of sample interval: a, 4 September 1979; b, 27
February 1980; c, 17 March 1981.

ship between these two measures of growth is shown in
Figure 3.

The x-intercepts of the regressions, where a linear pro-
jection would predict no growth, were consistently near
14 mm (% = 14.62 mm, SD = 0.52). At lengths over 14
mm, many Littorina angulifera grew in discrete episodes
separated by periods of no growth. Despite generally spo-
radic recovery of individuals, the growth of some snails

Y= 4.7x10 © + 6.28(X)
r2= 0.96 n=3912

Lip Growth/ day (mm)

O 0.03 0.09 0.15 0.21
Length Growth/ day (mm)

Figure 3

Littorina angulifera. Relationship between growth rates of shell
lip (Y) and length (X) using pooled data from all samples.

could be traced continuously up to and beyond the first
halt in lip growth. Examples (Figure 4), chosen to indicate
the variety of growth histories observed, show that the
initial cessation of growth could occur at a wide range of
lengths. The period of time over which individuals showed
no growth was variable, as were the duration and rate of
subsequent growth.

The growth coefficients of the small Littorina angulifera
varied over time but showed little seasonality (Figure 5a),
and were not correlated with rainfall (r = 0.06) or max-
imum water level (r = 0.04, both n = 26, P > 0.05).

Snails larger than 14 mm had a clearly seasonal pattern
of growth, with faster median growth rates (Figure 5b)
and greater proportions of growing individuals (Figure 5c)
between September and June, a period that includes all
of the dry season and much of the wet season. The growth
rates of the larger snails showed a negative correlation
with rainfall (r = —0.41, n = 42, P < 0.01) but were
independent of maximum water level (r = —0.06, n = 41,
P > 0.05).

The median growth rates of the larger Littorina angu-
lifera were correlated with the growth coefficients of the

The Veliger, Vol. 30, No. 1

es ee
Z wel
| }

13

Shell Length (mm)

Jan Jan Jan Jan Jan
1979 1980 1981 1982 1983

Figure 4

Littorina angulifera. Shell length at successive recaptures (+) for
nine snails initially marked at length <14 mm; each trace begins
at the first interval with no lip growth.

smaller snails (7 = 0.42, n = 26, P < 0.05). This was not
due to influxes of small, fast-growing snails into the larger
size class, because median lengths and growth rates in
samples of larger animals were not correlated (r = 0.02,
n = 42, P > 0.05).

The range of observed growth rates declined in 1982
(Figure 5b) owing to the termination of the marking pro-
gram. The proportions of growing snails also declined at
that time as the smaller individuals eventually stopped
growing, but as dry season approached most snails resumed
growth (Figure 5c).

Unmarked snails were found on the trees during each
collection. The rate of recruitment (Figure 5d) showed a
rising trend which paralleled the growth of the study trees.
Peaks in recruitment occurred twice each year, in late dry
season and in mid-wet season.

Growth of Tectarius muricatus

The relationship between length and growth rate in
Tectarius muricatus is most easily seen by combining all

Table 1

Product-moment correlations of four-week running means of the following weekly values: total rainfall (Rain), mean

daily insolation (Solar), mean daily salinity (Salin.), mean daily northerly wind energy (Wind), mean daily maximum

water level (Water), and mean daily maximum air temperature (Temp.). Number of data pairs used: Rain vs. Water,
229; Wind vs. Salin., 166; all others 211. Significance levels: **, P < 0.01; ns, P > 0.05.

Rain Solar
Rain =
Solar =O.0 7 —
Temp. O39 =0,30
Water —0.10 ns —0.12 ns
Wind =O O77
Salin. (0,711 0.80**

Temp. Water Wind Salin.
=0,.32" =

O72 0.42** —

0.25" —0.26** 0.50** —

J. M. Burgett et al., 1987

°
(oe)
N

S
°
a

0.03

Lip Growth/ day (mm) Growth Coefficient (K)

9°
hp

Proportion Growing
S Ou s
for) 0 fo)

fo)

2
—_

Recruits/ day

Page 17

Jul Jan Jul Jan Jul Jan Jul Jan Jul Jan
1979 1980 1981 1982 1983
Figure 5

Littorina angulifera. a. Growth coefficients (+95% confidence intervals) for snails <14 mm average shell length. b.
Growth rates of snails >14 mm average shell length: medians (points connected by line), quartiles (thick bars),
and ranges (thin bars). See Appendix 1 for sample sizes. c. Proportions (+95% confidence intervals) of snails >14
mm average shell length with growth since previous sample. d. Number of new (unmarked) snails in sample per

day of sample interval.

samples into a single scatterplot (Figure 6), because few
snails grew in each sample interval. Periods of no growth
were common at nearly all lengths, although snails smaller
than 14 mm were poorly represented. Most growth was

slow, and the maximum rates observed decreased with
increasing length. Growth rates of the smallest 7. muricatus
were comparable to those of Littorina angulvfera at similar
lengths. As in that species, lip extension rates of 7. murica-

Lip Growth/ day (mm)

9 13 17 21 25
Average Shell Length (mm)

Figure 6

Tectarius muricatus. Growth rate versus average of shell length
at start and end of interval, all samples combined. Rates recorded
from 4 June to 24 July 1985 (circles) to illustrate growth of
small snails were not used in analyses.

tus were linearly related to rates of length increase (7? =
0.92, n = 1549). The Model II regression formula was:

Lip extension = 1.2 x 10~° + 8.45(Length increase)

Growth histories of Tectarius muricatus (examples in
Figure 7) showed an episodic pattern similar to that of the
larger Littorina angulifera (Figure 3). Growth could resume
more than two years after cessation. Small increments in
length were not cumulative effects of slow growth, because
lip extension was rarely observed between episodes of mea-
surable increase in length. As in L. angulifera, the timing
and duration of growth episodes and the amount of growth
during an episode were variable, and not obviously related
to the length of the snail.

23
21
19

17

Shell Length (mm)

15

13
Jan Jan Jan Jan Jan
1979 1980 1981 1982 1983
Figure 7

Tectarius muricatus. Shell length at successive recaptures (+) for
four snails.

The Veliger, Vol. 30, No. 1

The median growth rates of the marked Tectarius muri-
catus were zero on all but two occasions (Figure 8a) owing
to the large proportion of non-growing animals in most
samples. The maximum growth rates in each sample were
positively correlated (r = 0.59, n = 34, P < 0.01) with
the proportion of animals growing, which varied between
zero and just over half of the animals sampled (Figure 8b).

Both maximum growth rates and the proportion grow-
ing peaked during wet seasons and appeared to reach
minima during dry seasons, although these data were sparse.
The proportion of snails growing showed a significant
correlation with rainfall (7 = 0.54, n = 34, P < 0.01) but
maximum growth rates did not (r = 0.22, n = 34, P >
0.05). Maximum water level was not correlated with either
maximum growth rates (r = 0.01) or with the proportion
growing (r = —0.13, both n = 34, P > 0.05).

DISCUSSION
Seasonal Patterns of Growth and Possible Causes

Consistent, annual cycles were found in the growth rates
of large Littorina angulifera and Tectarius muricatus at Ga-
leta. Despite the proximity of the study areas, the timing
of these cycles differed between the two species. The me-
dian growth rates of L. angulifera showed a broad peak
centered on the dry season, while the growth rates of T.
muricatus were slow at that time and fastest in the first
half of the wet season. Growth rates of the smaller L.
angulifera varied greatly, but with little evidence of a sea-
sonal pattern.

Seasonal changes in growth rates have been reported for
herbivorous gastropods both in temperate zones (¢.g.,
ORTON, 1928; FRANK, 1965a; SUTHERLAND, 1970; PHIL-
Lips, 1981) and in the tropics (e.g., FRANK, 1969; YaA-
MAGUCHI, 1977). In most cases the causes of this variation
are not known, but have been attributed to external factors
such as temperature (LARGEN, 1967; VERMEIJ, 1978;
EKARATNE & Crisp, 1984) or food supply (CusiT, 1984;
FLETCHER, 1984; UNDERWOOD, 1984a), or to internal fac-
tors such as costs of reproduction (ORTON, 1928; CoE &
Fox, 1942; BorKOwSKI, 1974; EKARATNE & CRISP, 1984).

Although minimum temperatures did not fluctuate sea-
sonally, peaks in maximum temperature coincided with
more rapid growth in Tectarius muricatus, a pattern also
observed in Florida by BORKOWSKI (1974). Because several
other physical factors had similar seasonal patterns (Figure
1, Table 1), no causal link can be inferred from this re-
lationship.

Experimental manipulations of densities of herbivorous
gastropods (SUTHERLAND, 1970; CREESE, 1980;
UNDERWOOD, 1984a; JERNAKOFF, 1985) and correlations
of algal abundance with their growth rates (SUTHERLAND,
1970; FLETCHER, 1984; UNDERWOOD, 1984a) suggest that
primary production may control growth rates in these graz-
ers. Because primary production depends upon the avail-
ability of moisture during daylight (JOHNSON et al., 1974),

J. M. Burgett et al., 1987

=
w

0.56 0.45 |

pe)

fo)
to

Lip Growth/ day (mm)
°

jo)

SS ©)
o [os]

Proportion Growing

ty

Jul Jan Jul Jan Jul
1979 1980

Page 19

0.46 |

.

Jan Jul Jan Jul Jan

1981 1982 1983

Figure 8

Tectarius muricatus. a. Growth rates: medians (points connected by line), quartiles (thick bars), and ranges (thin
bars). Medians were not calculated for sample sizes <10 (February and March 1980; see Appendix 2 for all sample
sizes). b. Proportions (+95% confidence intervals) of snails with growth since previous sample.

conspicuous blooms of algae high on shores are thought to
be partly due to seasonal increases in wetness of the sub-
stratum (LAWSON, 1957; CASTENHOLZ, 1961; NICOTRI,
1974; CusiT, 1984). The temporal patterns of wetness in
the two habitats studied here may have differed signifi-
cantly. Moisture retained in the porous coral rock of the
Tectarius muricatus study area may have increased the
abundance of epilithic and endolithic microalgae, which
colored the rock green during the wet season (J. Burgett,
personal observations). In the dry season, the more intense
wind and sun may have dried the surface layers of these
rocks despite wetting by the tides, thus reducing the supply
of food available to 7. muricatus.

In contrast to the strictly supralittoral Tectarius muri-
catus (BORKOWSKI, 1971; BANDEL, 1974), Littorina angu-
lifera grazes intertidal surfaces during nocturnal migra-
tions to lower levels of the mangroves (PLAZIAT, 1984; P.
Gutierrez, unpublished data). Although L. angulifera might
eat mangrove exudates or epiphyllic fungi, mangrove tissue
apparently is not ingested, as feeding behavior on clean
stems and leaves does not produce scrape marks (J. Bur-
gett, personal observations). Individuals on inert artificial
surfaces at Galeta grew to lengths of more than 25 mm,
apparently feeding on deposited material and (or) mi-
croalgae (J. Burgett & J. Cubit, personal observations).
Algal production on the surfaces of the mangrove roots,

which do not retain water, could follow a seasonal pattern
distinct from that on the higher coral wall. The relatively
non-seasonal pattern in the growth rates of the small L.
angulifera may be related to their remaining closer to the
water level than do the larger snails.

It is also possible that the availability of food for Tec-
tarius muricatus or Littorina angulifera was influenced by
other grazers, as competition has been shown to affect
grazing gastropods high on other intertidal shores
(UNDERWOOD, 1979, 1984b). Different sets of potential
competitors occurred in the two habitats. Other herbivores
in the rocky habitat of 7. muricatus were isopods (Ligia
sp.), crabs, terrestrial arthropods and the two species of
Nodilittorina. Although L. angulifera was the only grazer
we observed on supralittoral parts of Rhizophora, intertidal
areas of the trees are exposed to herbivorous fish and
invertebrates (BATISTA, 1980).

In some mollusks, the allocation of material and energy
to reproduction is thought to depress the rate of growth
(ORTON, 1928; CoE & Fox, 1942; BorKOowskKI, 1974;
EKARATNE & Crisp, 1984), although these processes can
occur simultaneously (LEIGHTON & BOOLOOTIAN, 1963;
PHILLIPs, 1981; CuBIT, 1984). In southern Florida
(25°30'N), LENDERKING (1954) observed Littorina angu-
lifera spawning through at least 10 months of the year (no
samples were taken in January or February). At this site,

Page 20

the wet season occurred between June and December. The
proportion of animals spawning was greatest in the spring
and autumn and least between December and March.

Our data show year-round recruitment, which would
be consistent with a long spawning season. If the repro-
ductive pattern of Littorina angulifera at Galeta is similar
to that reported from Florida, then shell growth and
spawning have broad, overlapping cycles, with alternating
peaks in the dry and wet seasons, respectively.

BORKOWSKI (1971) studied the reproductive cycle of Tec-
tarius muricatus in southern Florida, as LEwis (1960) did
to a lesser extent in Barbados (13°N), where the seasonal
patterns of rainfall and temperature were comparable to
those at Galeta (LEWIS et al., 1969). Tectarius muricatus
in Florida had ripe gonads from May to September, but
spawning was observed only between July and September
during extreme high tides, a pattern also shown by the
presence of egg capsules in plankton tows at Barbados
(Lewis, 1960). The annual growth pattern of 7. muricatus
reported from Florida (BORKOWSKI, 1974) coincides with
that observed at Galeta. If the pattern of reproduction in
Panama is similar to those at the other sites, then both
shell growth and gonadal development occur between May
and August, suggesting a large increase in available nu-
trients during the wet season.

Growth, Length, and Regional Comparisons

Littorina angulifera and Tectarius muricatus smaller than
14 mm grew faster than the larger snails that predominated
in the study populations. Small L. angulifera could add
more than 1 mm of lip per day (Figure 2c), while the
maximum rate seen in 7. muricatus was 0.6 mm per day
(Figure 6), similar to rates of L. angulifera of the same
length. These rates are about five times faster than those
reported from previous studies. LENDERKING’s (1954) data
on growth of L. angulifera over six weeks yielded a rate of
0.028 mm of length per day for snails 7.6 mm long (initial
length 7 mm), equal to 0.18 mm lip growth per day if the
ratio of length growth to lip extension was the same in
Florida as in Panama (Figure 4). BORKOWSKI (1974) re-
ported that 7. muricatus initially 11 to 12 mm in length
grew 0.017 mm per day over 60 days, equivalent to 0.13
mm of lip per day using his conversion ratio.

The processes causing latitudinal differences in growth
rates in these species and other prosobranchs (e.g., Tegula
funebralis Adams, 1855, by FRANK, 1975; Littorina neri-
toides Linnaeus, 1758, by HUGHES & ROBERTS, 1980)
remain obscure. Temperatures at the sites in southern
Florida were within the range of those at Galeta (BOR-
KOWSKI, 1971), but many other biotic and abiotic environ-
mental factors that could affect growth rates probably dif-
fered among sites. Genotypic clines have been proposed as
explanations for these patterns (FRANK, 1975), and gene
frequencies in L. angulifera are known to vary among
neighboring populations (GAINES e¢ al., 1974).

The Veliger, Vol. 30, No. 1

The rate of decline in growth rates for the smaller Lit-
torina angulifera was expressed by the parameter K of the
von Bertalanffy growth function. However, this function
was not an appropriate model for growth over the full
length range of either species. In addition to assuming an
asymptotic length where none may exist (KNIGHT, 1968),
the model requires that very small animals grow according
to the linear function. For L. angulifera (LENDERKING,
1954) and probably many other invertebrates, this as-
sumption does not hold (YAMAGUCHI, 1975). We, there-
fore, have used K solely as a convenient descriptor of the
linear rate of decline in growth rates of L. angulifera be-
tween 7 and 14 mm. Our plotting of growth rates against
average length rather than the more common initial length
gave closer estimates of growth rates at a given length
(LocKkwoobD, 1974), although it would not have been ap-
propriate for actual fitting of the model (YAMAGUCHI, 1975).
The GULLAND & HOLT (1959) method used here recently
has been found to underestimate K when Model I regres-
sion is used (SUNDBERG, 1984). By using a Model II regres-
sion technique and adjusting for variable sample intervals
by simulation, we have partially corrected for this bias.

A linear decline in growth rate with length implies a
length at which growth is zero. Although linearity past a
length of 14 mm was not tested, the values obtained were
consistent and close to the mean length (15 mm) at first
spawning of Littorina angulifera in Florida (LENDERKING,
1954). If the attainment of reproductive maturity coincides
with initial cessation of growth in L. angulifera, then this
length may be essentially constant with latitude, despite
the differences in growth rates of small animals. A similar
pattern has been reported in the trochid Tegula funebralis
(FRANK, 1975). The wide variation in the length at which
individuals of L. angulifera first stop growing (Figure 3)
may be related to gender. Females in Florida grew larger
in one year than did males (LENDERKING, 1954), although
in that paper it was unclear whether growth rates differed
among immature snails.

In Florida, Tectartus muricatus matured at the same
length as Littorina angulifera (BORKOWSKI, 1974). Thick-
ening of the shell lip, associated with temporary halts of
growth in other prosobranchs (LAXTON, 1970; FRANK,
1965b, 1969), was observed in 7. muricatus in Florida at
lengths of 13 to 16 mm (Singletary, in BORKOWSKI, 1974).
Our data support this range as the length at initial cessation
of growth in 7. muricatus in Panama. This species may
thus resemble L. angulifera in having rapid growth when
small, a temporary halt in growth at maturity, and sub-
sequent episodic growth.

Individual differences in growth rates were large enough
in both species to make length an unreliable indicator of
age. The median growth rates of both species were affected
by the varying proportions of growing animals in the sam-
ples. In Littorina angulifera, at least one-quarter, and often
all, of the snails in a sample grew, while no more than
one-half of the sampled Tectarius muricatus grew during

Je MesBurgettreyal Ney

any interval. In both L. angulifera and T. muricatus, females
have faster long-term rates of growth than do males
(LENDERKING, 1954; BORKOWSKI, 1974), suggesting that
some of the individual differences in episodic growth may
be sex-specific. If female L. angulifera grew more during
episodes, they would dominate the larger size classes, as
reported by LENDERKING (1954). However, because all L.
angulifera larger than 14 mm grew during some intervals,
males of this species must also grow episodically.

Episodic growth has been found in both tropical (FRANK,
1969) and temperate gastropods (e.g., ORTON, 1928;
LAXTON, 1970; SUTHERLAND, 1970; FRANK, 1975; HUGHES
& ROBERTS, 1980). This phenomenon may be common,
but it cannot be detected with measurements separated by
long intervals or by methods that average growth rates and
thus lose information from individuals. Detailed investi-
gation of growth patterns requires frequent measurements
of large numbers of individually identified animals. With
sufficient resolution, patterns of growth within and among
populations can provide a base for more analytical obser-
vations and experimental studies of physiological adap-
tations, food supply, phenology, and interactions among
species.

To our knowledge, Punta Galeta is at a lower latitude
than other sites from which seasonal growth rates of snails
have been reported. The asynchrony of the observed growth
patterns implies that no single overriding factor of the
environment controlled the growth of both Littorina an-
gulifera and Tectarius muricatus. The correlations of growth
rates with changes in the physical environment suggest
several explanatory hypotheses. These could be tested by
a combination of observational and experimental investi-
gations of, for example, competitive interactions, foraging
behavior, reproductive investment and timing, and abun-
dance of microalgae.

ACKNOWLEDGMENTS

We thank D. Windsor for summarizing the environmental
data, the Tropic Test Center of the United States Army
for solar radiation data, S. Williams and F. Chang for
marking and measuring snails, M. Fogarty for statistical
advice, S. Churgin and R. Sarmiento for help with ref-
erences, H. Caffey for figure preparation, and P. Gutierrez
for unpublished data. The manuscript was improved by
the comments of C. Brock, H. Caffey, P. Frank, K.
McGuinness, and an anonymous reviewer. This study was
supported by a grant to J. Cubit from the Environmental
Sciences Program of the Smithsonian Institution.

LITERATURE CITED

BANDEL, K. 1974. Studies on Littorinidae from the Atlantic.
Veliger 17:92-114.

BANDEL, K. & D. KapDousky. 1982. Western Atlantic species
of Nodilittorina (Gastropoda: Prosobranchia): comparative

Page 21

morphology and its functional, ecological, phylogenetic and
taxonomic implications. Veliger 25:1-42.

BaTisTA, V. 1980. Estudio de las comunidades que habitan las
raices del mangle rojo Rhizophora mangle L. de Punta Galeta,
Costa Atlantica de Panama. Dissertation, Fundacion Uni-
versidad de Bogota Jorge Tadeo Lozano, Bogota, Colombia.

BERTNESS, M. D. 1982. Shell utilization, predation pressure,
and thermal stress in Panamanian hermit crabs: an interoce-
anic comparison. Jour. Exp. Mar. Biol. Ecol. 64:159-187.

BorkowskI, T. V. 1971. Reproduction and reproductive peri-
odicities of south Floridian Littorinidae (Gastropoda: Pro-
sobranchia). Bull. Mar. Sci. 21:826-840.

Borkowskl, T. V. 1974. Growth, mortality and productivity
of south Floridian Littorinidae (Gastropoda: Prosobran-
chia). Bull. Mar. Sci. 24:409-438.

CASTENHOLZ, R. W. 1961. The effect of grazing on marine
littoral diatom populations. Ecology 42:783-794.

Cog, W.R. & D. L. Fox. 1942. Biology of the California sea
mussel (Mytilus californianus). Jour. Exp. Zool. 90:1-30.

CREESE, R.G. 1980. An analysis of distribution and abundance
of populations of the high-shore limpet, Notoacmea petterdi
(Tenison-Woods). Oecologia 45:252-260.

CusiT, J. C. 1984. Herbivory and the seasonal abundance of
algae on a high intertidal rocky shore. Ecology 65:1904-
1917.

Cusit, J.C. & S. WILLIAMS. 1983. The invertebrates of Galeta
Reef: a species list and bibliography. Atoll Res. Bull. 269:
1-45.

Cusit, J. D., D. M. Winpsor, R. C. THomMpson & J. M.
BURGETT. 1986. Water level fluctuations, emersion re-
gimes, and variations of echinoid populations on a Caribbean
reef flat. Estuar. Coast. Shelf Science 22:719-737.

EKARATNE, S. U. K. & D. J. Crisp. 1984. Seasonal growth
studies of intertidal gastropods from shell micro-growth band
measurements, including a comparison with alternative
methods. Jour. Mar. Biol. Assoc. U.K. 64:183-210.

FLETCHER, W. J. 1984. Intraspecific variation in the popula-
tion dynamics and growth of the limpet, Cedlana tramoserica.
Oecologia 63:110-121.

FRANK, P. W. 1965a. The biodemography of an intertidal snail
population. Ecology 46:831-844.

FRANK, P. W. 1965b. Shell growth in a natural population of
the turban snail, Tegula funebralis. Growth 29:395-403.
FRANK, P. W. 1969. Growth rates and longevity of some gas-
tropod mollusks on the coral reef at Heron Island. Oecologia

2:232-250.

FRANK, P. W. 1975. Latitudinal variation in the life history
features of the black turban snail Tegula funebralis (Proso-
branchia: Trochidae). Mar. Biol. 31:181-192.

GaInEs, M. S., J. CALDWELL & A. M. Vivas. 1974. Genetic
variation in the mangrove periwinkle Littorina angulifera.
Mar. Biol. 27:327-332.

GULLAND, J. A. & S. J. Hott. 1959. Estimation of growth
parameters for data at unequal time intervals. Jour. Cons.
Perm. Int. Explor. Mer 24:47-49.

Hay, M. E. & J. N. Norris. 1984. Seasonal reproduction and
abundance of six sympatric species of Gracilaria Grev. (Gra-
cilariaceae; Rhodophyta) on a Caribbean subtidal sand plain.
Hydrobiologia 116/117:63-94.

HENDLER, G. L. 1977. The differential effects of seasonal stress
and predation on the stability of reef-flat echinoid popula-
tions. Pp. 217-223. Jn: Proceedings, Third International
Coral Reef Symposium. University of Miami: Miami, Flor-
ida.

Page 22

HuGues, R. N. & D. J. RoBerTs. 1980. Growth and repro-
ductive rates of Littorina neritoides (L.) in North Wales. Jour.
Mar. Biol. Assoc. U.K. 60:591-599.

JERNAKOFF, P. 1985. An experimental evaluation of the influ-
ence of barnacles, crevices and seasonal patterns of grazing
on algal diversity and cover in an intertidal barnacle zone.
Jour. Exp. Mar. Biol. Ecol. 88:287-302.

Jounson, W. S., A. Gicon, S. L. GULMON & H. A. MOONEY.
1974. Comparative photosynthetic capacities of intertidal
algae under exposed and submerged conditions. Ecology 55:
450-453.

KAUFMANN, K. W. 1981. Fitting and using growth curves.
Oecologia 49:293-299.

KNIGHT, W. 1968. Asymptotic growth: an example of nonsense
disguised as mathematics. Jour. Fish. Res. Board Can. 25:
1303-1307.

LarRGEN, M. J. 1967. The influence of water temperature upon
the life of the dog-whelk Thais lapillus (Gastropoda: Pro-
sobranchia). Jour. Anim. Ecol. 36:207-214.

Lawson, G. W. 1957. Seasonal variation of intertidal zonation
on the coast of Ghana in relation to tidal factors. Jour. Ecol.
45:831-860.

Laxton, J. H. 1970. Shell growth in some New Zealand
Cymatiidae (Gastropoda: Prosobranchia). Jour. Exp. Mar.
Biol. Ecol. 4:250-260.

LEIGH, E. G., JR., A.S. RAND & D. M. WINDsor (eds.). 1982.
The ecology of a tropical forest: seasonal rhythms and long-
term changes. 468 pp. Smithsonian Institution Press: Wash-
ington, D.C.

LEIGHTON, D. & R. A. BOOLOOTIAN. 1963. Diet and growth
in the black abalone, Haliotis cracherodu. Ecology 44:227-
238.

LENDERKING, R. E. 1954. Some recent observations on the
biology of Littorina angulifera Lam. of Biscayne and Virginia
Keys, Florida. Bull. Mar. Sci. Gulf Caribbean 3:273-296.

Lewis, J. B. 1960. The fauna of rocky shores of Barbados,
West Indies. Can. Jour. Zool. 38:391-435.

Lewis, J. B., F. AXELSEN, I. GoopBopy, C. PAGE, G. CHISLETT
& M. CuoupHoury. 1969. Latitudinal differences in
growth rates of some intertidal marine molluscs in the Ca-
ribbean. Marine Sciences Manuscript Rept. No. 12. 89 pp.
McGill University, Montreal.

LockwoobD, S. J. 1974. The use of the von Bertalanffy growth
equation to describe the seasonal growth of fish. Jour. Cons.
Int. Explor. Mer 35:175-179.

Macintyre, I. G. & P. W. GLYNN. 1976. Evolution of modern
Caribbean fringing reef, Galeta Point, Panama. Amer. As-
soc. Petrol. Geol. Bull. 60:1054-1072.

McQuaip, C. D. 1981. Population dynamics of Littorina af-
ricana knysnaensis (Philippi) on an exposed rocky shore. Jour.
Exp. Mar. Biol. Ecol. 54:65-76.

NicoTri, M. E. 1974. Resource partitioning, grazing activities,

The Veliger, Vol. 30, No. 1

and influence on the microflora by intertidal limpets. Doc-
toral Thesis, University of Washington, Seattle, Washing-
ton.

OrTON, J. H. 1928. Observation on Patella vulgata, Part II.
Rate of growth of shell. Jour. Mar. Biol. Assoc. U.K. 15:
863-874.

PENNINGTON, M. 1983. Efficient estimators of abundance, for
fish and plankton surveys. Biometrics 39:281-286.

PHILLIPS, D. W. 1981. Life-history features of the marine
intertidal limpet Notoacmea scutum (Gastropoda) in central
California. Mar. Biol. 64:95-103.

PLAZIAT, J. C. 1984. Mollusk distribution in the mangal. Pp.
111-143. In: F. D. Por & I. Dor (eds.), Hydrobiology of
the mangal. Dr. W. Junk Publishers: The Hague.

RICKER, W. E. 1973. Linear regressions in fishery research.
Jour. Fish. Res. Board Can. 30:409-434.

ROSEWATER, J. 1970. The family Littorinidae in the Indo-
Pacific. Part I. The subfamily Littorininae. Indo-Pacif. Mol-
lusca 2:417-506.

SaLvaT, B. & M. DENizoT. 1982. La distribution des mol-
lusques supralittoraux sur substrats carbonates tropicaux
(Polynésie Frangaise) et leur regime alimentaire. Malaco-
logia 22:541-544.

SoKAL, R. R. & F. J. ROHLF. 1981. Biometry. The principles
and practice of statistics in biological research. W. H. Free-
man & Co.: San Francisco. 776 pp.

SUNDBERG, P. 1984. A Monte Carlo study of three methods
for estimating the parameters in the von Bertalanffy growth
equation. Jour. Cons. Int. Explor. Mer 41:248-258.

SUTHERLAND, J. 1970. Dynamics of high and low populations
of the limpet, Acmaea scabra (Gould). Ecol. Monogr. 40:
169-188.

UNDERWOOD, A. J. 1979. The ecology of intertidal gastropods.
Adv. Mar. Biol. 16:111-210.

UNDERWOOD, A. J. 1984a. Microalgal food and the growth of
the intertidal gastropods Nerita atramentosa Reeve and Bem-
bictum nanum (Lamarck) at four-heights on a shore. Jour.
Exp. Mar. Biol. Ecol. 79:277-291.

UNDERWOOD, A. J. 1984b. Vertical and seasonal patterns in
competition for microalgae between intertidal gastropods.
Oecologia 64:211-222.

VAN DEVENDER, R. W. 1978. Growth ecology of a tropical
lizard, Basiliscus basiliscus. Ecology 59:1031-1038.

VERMEYJ, G. J. 1978. Biogeography and adaptation: patterns
of marine life. Harvard University Press: Cambridge. 332
PP-

YAMAGUCHI, M. 1975. Estimating growth parameters from
growth rate data: problems with marine sedentary inverte-
brates. Oecologia 20:321-332.

YAMAGUCHI, M. 1977. Shell growth and mortality rates in the
coral reef gastropod Cerithium nodulosum in Pago Bay, Guam,
Mariana Islands. Mar. Biol. 44:249-263.

J. M. Burgett et al., 1987 Page 23

Appendix 1 Appendix 2

Littorina angulifera. Sample dates (day/month/year), Tectarius muricatus. Sample dates (day/month/year),
number of snails used in analysis of each size class (7), number of snails used in analysis (7), and number of days
and number of days since previous sample (Interval). Data since previous sample (Interval). Data following intervals
following intervals >50 days (*) were not used in analyses. >50 days (*) were not used in analyses.
Date n (S14 mm) n (>14 mm) Interval Date n Interval
23/10/78 8 62 33 6/7/78 a? 181
24/11/78 5 68 32 11/8/78 17 36
3/1/79 20 67 40 14/9/78 36 34
13/2/79 7 68 41 23/10/78 31 39
19/3/79 3 54 34 28/12/78 faye 66
27/4/79 1 44 39 28/3/79 tO 90
29/5/79 9 48 32 5/10/79 17 43
1/7/79 20 64 34 6/15/79 27 36
2/8/79 38 59 31 WAY UY D5 32
4/9/79 38 61 33 22/8/79 28 36
19/10/79 19 74 45 11/10/79 30 50
26/11/79 9 57 38 14/11/79 22 34
21/1/80 9* 61* 56 7/1/80 9* 54
27/2/80 35 88 37 14/2/80 6 38
9/4/80 46 87 42 26/3/80 9 41
11/5/80 23 102 32 28/4/80 30 33
10/6/80 16 88 30 28/5/80 36 30
21/7/80 i 13 41 27/7/80 B25 60
24/8/80 19 70 34 14/9/80 36 49
21/9/80 36 96 28 19/10/80 37 35
22/10/80 27 47 31 17/11/80 17 29
19/11/80 25 59 28 22/1/81 IS 65
12/1/81 Lil Die 53 25/2/81 29 34
17/2/81 20 55 36 30/3/81 28 33
17/3/81 39 81 28 10/6/81 Sie 72
27/5/81 8* 2% 71 23/7/81 377) 43
1/7/81 29 103 35 26/8/81 36 34
29/7/81 42 103 28 24/9/81 41 29
31/8/81 45 50 33 26/10/81 46 32
28/9/81 47 97 28 24/11/81 37 29
30/10/81 50 90 32 13/1/82 29 50
3/12/81 44 115 34 18/2/82 33 36
7/1/82 19 125 35 24/3/82 29 34
4/2/82 33 148 28 21/4/82 24 28
5/3/82 30 14 29 1/6/82 23 41
14/4/82 23 129 40 8/7/82 28 By
18/5/82 10 103 34 10/8/82 51 33
16/6/82 5 91 29 10/9/82 57 31
14/7/82 1 68 28 15/10/82 43 35
17/8/82 1 68 34 2/12/82 38 48
17/9/82 1 59 31 10/1/83 94 39
19/10/82 0) 43 32 16/2/83 68 Shi/
30/11/82 0) 26 42 23/3/83 50 35
4/1/83 0 26 35
7/2/83 0) 19 34

The Veliger 30(1):24-39 (July 1, 1987)

THE VELIGER
© CMS, Inc., 1987

Courtship and Dart Shooting Behavior of the
Land Snail Helix aspersa
by

DANIEL J. D. CHUNG!

Division of Biological Sciences and Museum of Zoology,
University of Michigan, Ann Arbor, Michigan 48109, U.S.A.

Abstract. The dart apparatus, found in a number of pulmonate and opisthobranch gastropods,
contains a dart that is used to pierce the flesh of a partner during courtship and mating. It has usually
been assumed that dart receipt somehow “stimulates” co-operative courtship behavior, but previous
studies have been unable to confirm this hypothesis. In this study, the courtship and dart shooting
behavior of the stylommatophoran Helix aspersa Muller was studied in order to document in detail the
courtship of this snail and to determine whether dart receipt stimulates courtship or has another function.
As in H. pomatia, there are two basic courtship sequences in H. aspersa: one in which dart shooting
behavior occurs and one in which it is omitted. The courtship sequence is determined solely by the
internal condition of the snail. Young snails have courtship behavior that differs slightly from that of
older snails. Quantitative tests show that dart receipt has no effect on the fraction of time spent out of
genital contact or the mean rate of biting, but dart receipt appears to decrease the rate of attempted
copulation. Dart shooting, by contrast, appears to stimulate the shooter into attempting copulation and
into decreasing its rate of biting. It is theorized that the dart may have evolved as a result of sexual
selection in hermaphrodites to coerce a mate into acting more as a “female” or to prevent a mate from

“cheating” as a “male.”

INTRODUCTION

The dart apparatus is a set of organs found in the terminal
genitalia of a number of hermaphroditic pulmonate and
opisthobranch gastropods. The dart apparatus consists of
one or more dart sacs containing a dart—a chitinous or
calcareous spear that is thrust into the flesh of a courting
partner during “dart shooting” —and associated glands. In
general, there are two basic types of dart apparatuses: those
with hollow darts perforated at the tip and with a gland
at its base, which may be used as hypodermic devices, and
those with darts not perforated at the tip and with glands
(“mucous glands’’) near the base. Helicids have the latter
type of dart apparatus. Helicids also have deciduous darts;
that is, they are cast off during dart shooting and replaced
shortly after courtship. It is possible that all non-helicid
dart-bearing snails possess non-deciduous darts. Darts may
have evolved independently in the helicaceans, ariophan-
taceans, zonitaceans, philomycids, soleoliferans, nudi-
branchs, and possibly cephalaspideans and cavoliniids (see

' Mailing address: 3324 Wiliama Place, Honolulu, Hawaii
96816, U.S.A.

Tompa, 1980; PRUvoT-FOL, 1960). It has usually been
assumed that the dart somehow “stimulates” the courting
partner (see Tompa, 1980, for review), although courtship
observations have not been able to demonstrate any func-
tion for the dart.

Observations on courtship behavior, with descriptions
of dart shooting or use of the dark apparatus, in dart-
bearing land snails have been given for a number of species,
including: the helicids Helix pomatia Linnaeus (MEISEN-
HEIMER, 1912; LIND, 1976; JEPPESEN, 1976), H. aspersa
Muller (HERZBERG & HERZBERG, 1962); GIUSTI & LEPRI,
1980), Eobania vermiculata (Miller), Tacheocampylaea
tacheoides (Pollonera), H. lucorum (Linnaeus) (GIUSTI &
LeEpRI, 1980); the bradybaenid Eulota fruticum Muller
(KUNKEL, 1928); the vitrinids Vitrina elongata Draparnard
(KUNKEL, 1933), V. brevis Ferussac (KUNKEL, 1929, 1933),
V. major Férussac (GERHARDT, 1935; see also FORCART,
1949); the parmacellid Parmacella deshayest Moquin-Tan-
don (GERHARDT, 1935); the zonitid Ventridens Binney
(WEBB, 1948, 1968b); the helminthoglyptids Helmintho-
glypta Ancey (WEBB, 1942, 1951, 1952b), Monadenza Pils-
bry (WEBB, 1952a), Cepolis Denys de Montfort (WEBB,
1952b), Humboldtiana ultima Pilsbry (WEBB, 1980); the

ID); Jfa ID), Charreys, WOS7/

philomycid Philomycus carolinianus (Bosc) (WEBB, 1968a);
and the ariophantids Ariophanta ligulata (Ferussac) (Da-
SEN, 1933), Macrochlamys pedina (Benson) (RENSCH, 1955),
and M. indica Godwin-Austen (RAUT & GHOSE, 1984).
With the exception of the studies of LIND (1976) and
JEPPESEN (1976), these reports are primarily brief descrip-
tive accounts of courtship.

LIND (1976) provided a detailed ethological analysis of
courtship and mating behavior in Helix pomatia and at-
tempted to determine the role of dart shooting in the overall
courtship sequence through a quantitative analysis of be-
haviors (1) before and after receipt of a dart and (2) be-
tween snails that received versus snails that did not receive
a dart. Lind found that dart receipt was not a prerequisite
for completion of courtship and copulation and that dart
receipt at best appeared to have a slightly negative effect
on courtship activity. He found some evidence that dart
receipt harmed snails and caused cessation of courtship.
JEPPESEN (1976) obtained similar results from observa-
tions of courtship in H. pomatia that had the dart sac or
mucous glands surgically removed.

The more descriptive reports of courtship and dart
shooting in land snails provide little evidence for any spe-
cific function of dart shooting. WEBB (1952b) suggested
that the dart was used by a snail to force its partner to co-
operate in courtship by inducing sexual excitement and
also to prevent the partner from biting or harming the dart
shooter’s everted genitals. KUNKEL (1929, 1933) believed
that the dart apparatus in Vitrina major was a holdfast
organ operating by suction, although GERHARDT (1935)
could not verify this hypothesis.

The study reported here is an attempt to understand
the function of the dart apparatus through behavioral ob-
servations of dart shooting during the courtship of Helix
aspersa. This study describes in detail the courtship of H.
aspersa, which had previously been reported in only cur-
sory fashion by GrusT1 & LEpRI (1980) and HERZBERG
& HERZBERG (1962), and tests the hypothesis that dart
receipt has a stimulatory effect on courtship behavior.

MATERIALS anp METHODS

Specimens of Helix aspersa were obtained from College
Biological Supply (Escondido, California). The snails were
individually isolated in small plastic containers lined with
soil and were provided with egg shells and carrot slices.
Snails were kept at 21-26°C under a 12 h light: 12 h dark
photoperiod for at least two months before being used in
courtship observations. This period of isolation appeared
to increase the likelihood of snails courting when put to-
gether again. Only fully adult snails with a reflected lip
and deflected body whorl were used for descriptions of
courtship and quantitative analysis of courtship behavior.
Courtship in young snails (defined as “‘subadults” on the
basis of conchological characters—large snails without a
reflected lip) was observed for qualitative comparison with
courtship in older snails. The subadult snails were all

Page 25

virgins, having been raised from an early juvenile stage in
isolation. The field-collected adult snails had an unknown
history.

Detailed quantitative observations of courtship were
made on 60 pairs of snails, and qualitative observations
were made on the courtship and mating of more than 40
other pairs. Of these more than 100 pairs, 10 were pairings
of subadults. Of the 60 pairs observed in detail, the data
for 36 pairs were detailed enough for quantitative analysis
of behaviors presumably related to dart shooting.

Observations on courtship behavior of isolated pairs were
taken at night in a lighted room. For each observation
session about 12 snails were removed from isolation, washed
in water, and placed in an “introductory arena” (a trans-
parent plastic box) where the crawling snails could be
observed to identify which snails would court. Snails that
exhibited slight eversion of the genitals were noted, and
pairs of these snails were transferred to an “observation
arena” (a smooth plastic lid, 18 x 13 cm, with upturned
sides 2 cm high). Recording of courtship behavior was
begun as soon as the pair was placed in the center of the
arena and was terminated after the snails attained intro-
mission, one (or both) of the snails withdrew from court-
ship by crawling out of the arena, or courtship was ter-
minated by the observer. Behavioral records were made
on a 20-channel recorder or on a pocket card printer with
numerical codes for defined acts. Terminations by the ob-
server were confined to cases where snails had difficulty
attaining intromission after 30 min of attempted copula-
tion.

Observations were made on snails courting upright on
a horizontal surface. Although snails often mate upside
down on the ceilings of laboratory containers, courtship
does not appear to be affected by physical orientation to
their substrate.

Statistical tests were performed on behavioral data (see
below). as described in CONOVER (1980) and SOKAL &
ROHLF (1969).

LIST of BEHAVIORS RECORDED
IN COURTSHIP

Labial-head contact (LH) (Figure 1A) occurs when a snail
probes the head and labial region of another snail with its
mouth and labial palps. The head of the snail is raised off
of the substrate, and its tentacles are fully extended. The
snail moves its jaws and radula actively, and intermittently
bites its partner or nuzzles it. Reciprocation appears to be
necessary for prolonged LH behavior. The genital pore
shows some swelling, or the genitals may be partially
everted.

Labial probing of the region of the genitals (LG) (Figure
1C) occurs when a snail presses its mouth and labial palps
on the genitals or on the skin next to the genitals of the
partner. The oral probing is focused primarily in a region
just posterior to the genital pore of the partner. This be-
havior can occur with or without genital eversion of either

Page 26

The Veliger, Vol. 30, No. 1

Figure 1

Courtship behavior in Helix aspersa. A. Labial-head contact. B. Interruption of courtship. C. Labial-genital contact.
This pair is in LG-1. D. IDS behavior is shown by the snail on the left; the snail on the right shows LG behavior.

the actor or recipient, although full genital eversion usually
begins at this time. A full genital eversion occurs when
the atrium is evaginated and swollen, and the female (va-
ginal, anterior) and male (penial, posterior) openings are
visible. When the behavior occurs simultaneously and re-
ciprocally in both snails, the everted genitals will be ap-
pressed and apposed. Genital apposition was not regarded
as a separate behavior and was regarded as a result of the
simultaneous orientation of the two partners in LG contact,
because orientation of the snails towards each other did
not appear to depend on genital apposition. LG behavior
occurred before and after dart shooting, although with
different consequences. LG behavior before dart shooting
(LG-1) could not be distinguished from LG behavior after
dart shooting (LG-2) except that each led to different
behavioral acts in the courtship sequence.

Intention of dart shooting (IDS) (Figure 1D, snail on the
left) is a behavior that is seen immediately before dart
shooting; the term is borrowed from LIND (1976). A snail

showing well-developed IDS behavior has shortened (but
not invaginated) tentacles, a swollen and distended anterior
head foot, very swollen and turgid genital eversion with a
distension of the anterior (vaginal) region (where the dart
sac is located), and a sole that is contracted and reduced
in size. The snail in IDS pushes its everted genitals against
its partner in a constant pushing motion. There appears
to be no oral probing by the snail in IDS of its partner.
The everted genitals and anterior headfoot are more swol-
len at this time than at any other time in courtship; this
may be due to increased hydrostatic pressure caused by
tensing of the body musculature of the foot and posterior
headfoot. IDS persists only as long as the genitals are
maintained in contact with the partner’s body. The ever-
sion may be pressed against any area of the partner, in-
cluding the shell, and the pushing may result in the partner
even being swept off the substrate and onto the snail in
IDS. IDS is terminated by dart shooting. Occasionally, a
snail may show very little or essentially no IDS behavior

D. J. D. Chung, 1987

Page 27

Figure 2

Courtship behavior in Helix aspersa. A. Dart shooting behavior shown by snail on the left. The dart of the snail
did not penetrate well the partner and was withdrawn back into the dart sac. B. Penial eversion (AC) shown by
snail on the right. C. Both snails going through AC. Note the swollen genitals. D. Copulating snails. Both snails

have taken the “mating posture.”

before dart shooting. Young snails have poorly developed
IDS behavior (see below).

Dart shooting (DS) (Figure 2A) occurs when a snail
quickly everts the basal tubercle of the dart sac out of its
everted genitals. The dart, which is attached by its base
to the tubercle in the base of the dart sac, is rapidly pushed
from the dart sac and usually pierces the flesh of the
partner. Virgin snails possess no dart (see Discussion), and
DS behavior leads only to the rapid eversion of the fleshy
tubercle in these snails. The eversion of the tubercle takes
a fraction of a second, and withdrawal of the tubercle takes
3-10 sec. The dart is never propelled through the air,
because it is firmly attached by its base to the tubercle
until it is lodged in the partner’s tissues. Once lodged in
the partner, the dart is detached from the tubercle and is
left in the partner. Occasionally, the dart either does not
hit the partner or it does not lodge in the flesh and is

withdrawn partially or entirely back into the dart sac. Once
DS behavior has occurred, the dart is never used again.
Dissections of snails that had withdrawn their darts back
into the dart sacs showed that these darts are discarded
into the bursal diverticulum shortly before reception of a
spermatophore from the partner during copulation. A new
dart starts to grow within 6 h after expulsion of a dart
and is fully grown within 5 to 7 days after DS (see DIL-
LAMAN, 1981; Tompa, 1982). During the expulsion of the
dart, a globule of whitish mucus, probably from the mucous
glands, is usually seen adhering to the dart. Immediately
after DS, a snail may evert its penis once.

Penal eversion and attempted copulation (AC) (Figure
2B). Penial eversion occurs repeatedly until a snail either
achieves intromission or courtship is broken off. In the
normal development of AC behavior, the snail, while ori-
ented with its everted atrium pressed against the body of

Page 28

the partner, exhibits a momentary tensing of the body wall
of the anterior headfoot. This is followed immediately by
increased turgescence of the everted atrium and then by
penial eversion. The everted penis (about 5-10 mm long)
invaginates immediately if the snail does not achieve suc-
cessful intromission; the total act takes less than 10 sec.
After the act is over, the snail pauses before attempting
copulation again. Normally, the everted atrium of a snail
is pressed against the everted atrium of its partner (z.e.,
the genitals are apposed) when AC occurs. However, a
snail can also evert its penis when the everted atrium is
pressed against the tail, shell, or any other part of its
partner. Thus, tactile stimulation of the genitals appears
to be necessary for AC behavior to be triggered.

Copulation (C) (Figure 2D) was defined by the exter-
nally observable behavior of obtaining successful intro-
mission and adoption of the “mating posture.” The de-
position of sperm in the partner could usually not be verified
without dissecting the partner after copulation. In suc-
cessful intromission, the everted penis of a snail is allowed
to penetrate the vagina of a partner and to lodge in the
vaginal canal. The snail attaining intromission takes on
the mating posture, where the head is lifted off the sub-
strate, the tentacles are shortened and held vertically, and
the snail remains immobilized until it deposits its sper-
matophore into the partner’s bursal diverticulum.

In dissected specimens, the intromitted penis (about 2
cm long) is found to lie in the vagina of the partner; the
swollen, bulbous head of the penis is lodged at the base of
the bursal (spermathecal) stalk and free oviduct. Thirty
minutes after achieving successful intromission, the penis
is anchored in the vaginal canal to the extent that the snails
cannot be pulled apart without physical injury. In this
study, if a snail had intromitted and maintained the mating
posture for at least half an hour, it was assumed to have
gone on to complete copulation.

Tail following (TF). A snail showing tail following be-
havior follows the tail of its partner, either touching the
tail with its oral region or closely following the tail. It is
possible that a snail showing TF behavior is following the
mucous trail of the partner, but this could not be deter-
mined with certainty. Usually, TF behavior is non-recip-
rocal, but occasionally two snails will follow one another’s
tail in a circle which eventually tightens up and leads to
the snails meeting head to head.

Pauses (P). During a pause, a snail stops courtship ac-
tivity, does not crawl around, and does not have its head
oriented towards its partner. The snail may move its mouth
or rasp at the mucus on the substrate. If it has an eversion,
the eversion may decline. The muscles of the body are not
tensed and the anterior headfoot is not swollen.

Biting (B). Biting was recorded as a separate act during
any part of courtship outside of LH contact. The biting
snail makes rasping movements against the skin of the
partner, and the partner reacts by retracting slightly after
each bite.

The Veliger, Vol. 30, No. 1

Interruptions (1) (Figure 1B). During an interruption,
a snail crawls away from the partner. The snail may make
a tight circling pivot and return within a few seconds, or
the snail may crawl far away from the courtship spot. A
long interruption may lead to withdrawal from courtship.
If a snail has an eversion, the eversion declines.

Withdrawal from courtship (W) occurs when a snail ceas-
es all courtship behavior, persistently avoids all contact
with its partner, and crawls away from the courtship site
and out of the observation arena.

COURTSHIP SEQUENCE

Two types of courtship sequences are observable in fully
mature Helix aspersa: primary courtship and secondary
courtship (Figure 3; terms from LIND, 1976). In addition,
the courtship behavior in young snails just mature enough
to court is qualitatively slightly different from that of fully
mature snails.

A primary courtship sequence (Figure 3A) includes dart
shooting behavior and is seen in courting snails with a
fully formed dart and in virgin snails (which possess no
dart) courting for the first time. A secondary courtship
sequence (Figure 3B) does not include IDS or DS behavior
and is seen in snails that have not yet fully grown a re-
placement for a dart shot in a previous courtship attempt.
Whether or not a snail goes through a primary or a sec-
ondary courtship sequence appears to depend solely on the
internal state of the animal and is not altered by the be-
havior of the partner it is courting. Thus, one snail of a
courting pair may go through a primary courtship se-
quence while its partner may go through a secondary court-
ship sequence.

Orientation towards the partner in courtship occurs
principally by physical contact with the tentacles and oral
region, although some orientation towards mucous trails
or the thick patch of mucus that develops at the courtship
site may also occur. Orientation towards the partner and
a certain amount of synchrony in behavior is necessary for
courtship to continue.

Primary Courtship Sequence

The behavior sequences of 34 pairs of snails are sum-
marized in a simplified diagram (Figure 3A). These snails
were part of a group of 36 pairs used for quantitative
analysis in this study. The number of pairs in which the
acting snail made a transition from one behavior to another
in the sequence is given next to each arrow. The diagram
says nothing about the synchrony or lack of synchrony
between the partners. However, because the snails are
simultaneous hermaphrodites, and both snails go through
the same basic sequence, the numbers given are those for
pairs and not individuals.

The diagram does not show pauses, and it does not show
two atypical pairs: (1) one pair in which a snail in LG-1
withdrew from courtship after its partner (which had no

Dap De Chung, 1987

A.

PNY’

Page 29

B !

\ fo. Ve
28 4

terminated
gf by observer

cg | fl amecootee |. G- 4mmigs IDS EE a ee 9 wee AC aaa C

awe

23 mutual
11 1 unilateral

TF

| Phase | | |

LH =—.e LG ae AC = C

Figure 3

Diagram of courtship behavior in Helix aspersa. The number of courting pairs making the transition from one
behavior to another is shown next to the arrow. Behaviors of actors (not recipients) are shown. Pauses are not
shown. Complicated interactions between B, I, and TF are for the most part not shown. 3A. Primary courtship
sequence. 3B. Simplified diagram for secondary courtship sequence. Biting, interruptions, withdrawals, and tail
following not shown. LH, labial-head contact; LG-1, labial-genital contact before dart shooting; IDS, intention of
dart shooting; DS, dart shooting behavior; LG-2, labial-genital contact after DS; AC, attempted copulation (penial
eversion); C, copulation; B, biting; I, interruption; TF, tail following; W, withdrawal from courtship.

dart) went through DS, and (2) a pair in which one snail
ejaculated alone without copulating (ignoring its partner)
after going through DS. Observations on 4 of the 28 pairs
reaching AC were terminated when it was noticed that
they had great difficulty achieving mutual intromission.
Although these four pairs probably would have eventually
attained intromission, the terminations are indicative of
the number of snails having difficulty in synchronizing
their behavior to effect copulation.

The courtship sequence is basically linear (Figure 3A).
There are three phases in primary courtship: (1) an in-
troductory phase (Phase I) which consists of LH behavior,
(2) a dart shooting phase (Phase II) which consists of LG
behavior (LG-1) leading to DS, and (3) a copulation phase
(Phase III) which consists of repeated AC during LG
behavior (LG-2) leading to successful intromission.

The diagram of courtship behavior for 34 pairs shown
in Figure 3A accurately reflects the variation in courtship
behavior of this species. The behavior sequence and certain
aspects of courtship related to DS behavior are fairly rigid.
Observations of more than 150 courting snails indicate
that DS is not a conditional behavior and always occurs
in snails with a fully formed dart and in virgin snails
courting for the first time. The timing of AC in the court-

ship sequence also appears to be rigid; AC occurs only
after the actor has gone through DS and does not depend
on receipt of a dart from its partner. The timing of with-
drawals may also be constrained; it is noticeable in Figure
3A that no snail withdrew from courtship after it had gone
through DS; withdrawals late in courtship may be rela-
tively rare.

Variation in courtship behavior in Helix aspersa is seen
chiefly in (1) the number of bites (B), interruptions (1),
and TF episodes, (2) the degree of development of IDS
behavior, (3) the type of dart wound, (4) the number of
AC occurring before copulation, and (5) the success of
mutual, reciprocal intromission during copulation.

IDS behavior can be virtually absent, partially devel-
oped (in young snails), or be fully developed. Omission of
IDS behavior was found to be significantly associated with
known and presumed virgin snails (snails without darts
going through DS): only 5 of 14 snails (36%) showing no
IDS possessed darts, while 38 of 44 snails (86%) showing
IDS possessed darts (P < 0.01, two-tailed Fisher’s exact
test).

In snails showing normal IDS behavior, maintenance
of IDS appears to depend, in part, on the partner’s move-
ments. A snail in IDS pushes indiscriminately against the

Page 30

partner’s body and does not orient itself well towards its
partner. If the partner does not orient itself towards the
snail in IDS, physical contact with the genitals of the snail
in IDS will be lost and IDS will cease. Thus, the partner’s
movements, in large measure, determine where in its body
it receives a dart.

Whereas DS behavior always occurs in a primary court-
ship sequence, the degree and location of dart penetration
into the partner varies. In a group of 42 darted snails,
penetration varied as follows: the dart was completely lost
in the hemocoel of 6 snails (14%), pushed partly into the
body and left there in 26 snails (62%), or pushed partly
into the body but then withdrawn back into the dart sac
of the shooter in 10 snails (24%).

In a group of 57 darted snails, the location of dart
penetration varied as follows: 2 snails were darted on the
left side of the headfoot (3%); 8 snails were darted on the
right side of the headfoot, anterior to the genitals (z.e., in
the head) (14%); 19 snails were darted on the right side
of the headfoot, posterior to the genitals (33%); 4 snails
were darted in the sole close to the mouth or on the mouth
(7%); 16 snails were darted in the sole away from the
mouth (28%); 1 snail had the dart pierce its everted penis
(2%); 1 snail was darted in the penial lobe (2%); 5 snails
were darted in the vaginal lobe (9%); and 1 snail was not
hit by the dart at all (2%). None of the five darts that hit
the vaginal lobe penetrated well; the darts penetrated less
that 2 mm and fell out. This may have been due to the
fact that the vaginal lobe includes the collar of the dart
sac, which is hardened with numerous, tiny calcium car-
bonate crystals (see TOMpPaA, 1982). In contrast, in only 3
of the 16 snails darted in the sole and in only 1 of the 19
snails darted in the headfoot posterior to the genitals did
the dart penetrate poorly and fall out.

Snails that go through DS behavior but have no dart
are virgins and do not inflict a wound on their partners;
these snails will begin to grow a dart after this first attempt
at DS (see CHUNG, 1986b).

The timing of DS—both the time from the start of
courtship to DS and the relative synchrony of DS behavior
between partners—is also variable (see quantitative anal-
ysis below).

Spermatophore release and reception almost always oc-
cur in the context of reciprocal and simultaneous intro-
mission. However, a few pairs intromit non-reciprocally—
“unilateral copulation,” with one male- and one female-
acting snail (3 of 71 pairs, or 4%)—and a few snails were
observed to take on the mating posture without intromit-
ting and to ejaculate without a partner, after an otherwise
normal courtship (2 of 88 snails, or 2% of individuals).
Self-copulation was never observed.

The behavior of snails in AC indicates that copulation
is not attained until a snail allows intromission by its
partner, and it appears that a snail will normally not allow
intromission unless it too achieves intromission at the same
time. Copulation cannot apparently be forced on an un-

The Veliger, Vol. 30, No. 1

willing partner in these snails, because the entrance to the
vagina is normally closed by a sphincter muscle, which is
relaxed only when the snail is also everting its own penis,
and the closed sphincter cannot be penetrated by the soft
penis. Simultaneous intromission is complicated by the fact
that snails of a courting pair rarely shoot darts simulta-
neously (see below), and thus AC behavior following DS
is not synchronized between the snails until after both have
gone through DS behavior. To attain copulation, two snails
must have their genitals perfectly apposed, go through AC
simultaneously, and allow intromission of the partner. The
momentary turgescence of the everted genitals immediately
preceding AC may be a tactile cue or a stimulus to trigger
AC in the partner. However, in spite of this possible cue,
AC frequently fails. Transient unilateral intromission is
frequent but is almost always terminated. When a snail
gains unilateral intromission, it assumes the mating pos-
ture, but the partner does not go into the mating posture
and immediately pulls away from the first snail or bites
at its penis until it is dislodged, or it “ejects” the penis,
with the penis appearing to be shoved out of the vagina.

Snails ejaculating without a partner and those allowing
unilateral copulation (female-acting snails) behaved sim-
ilarly to each other in that both acted as though they had
attained intromission, although they had failed to penetrate
their partners during AC. These snails attempted copu-
lation with their partners, failed to intromit successfully,
and then went into the mating posture with their penes
everted slightly (3 mm long) and projected anteroventrally.
The snails that mated non-reciprocally either remained in
the mating posture until they expelled their spermato-
phores from their penes onto the ground or they eventually
came out of the mating posture after 30 min and quietly
coupled with their male-acting partners. Because it takes
about 30 min for the penis to be anchored and effectively
locked in the vaginal canal, it was assumed that these
female-acting snails had no alternative but to remain united
with their partners after 30 min had passed. The few snails
taking on the mating posture without obtaining intromis-
sion were considered to be behaving abnormally; snails
that did this did not appear to be morphologically abnor-
mal.

The duration of primary courtship varies considerably.
The time from start of courtship to DS averages 35 + 19
min (¥ + SD; n = 63 snails, range: 1-75 min). The time
from DS to C usually takes 15-45 min, although a few
pairs take more that 4 h to attain copulation after both
have gone through DS.

Copulation was not studied in detail and was marked
by little external behavior. The duration of copulation was
not recorded for most snails but was observed to last from
4 to over 12 h. In a sample of 20 pairs, spermatophores
were found forming in the penial flagellum and penis
between 1 and 6 h after start of copulation. Transfer of
the spermatophore from the penis to the bursal divertic-
ulum of the partner occurs slowly over the last half of the

D. J. D. Chung, 1987

copulatory period and is usually not strictly simultaneous
for both snails. Once a snail transfers its spermatophore,
it comes out of the mating posture, retracts its penis, and
waits for its partner to finish.

Secondary Courtship

Secondary courtship is seen only in snails that have gone
through DS within the previous 5-7 days and have not
yet grown a fully formed dart in the dart sac. These are
snails that either have recently mated or recently gone
through an unsuccessful courtship (through DS). Second-
ary courtship was not analyzed quantitatively. It is essen-
tially like a primary courtship sequence without a dart
shooting phase (Figure 3B) and is of much shorter duration
than primary courtship. The first phase is an introductory
phase that is qualitatively like the introductory phase of
primary courtship. The second phase is a copulation phase
that is also qualitatively like the copulation phase in pri-
mary courtship. Helix aspersa has the ability to mate twice
within a 24-h period (one primary and one secondary
courtship) and pass two full spermatophores to its partners.
This does not occur frequently, as the majority of snails
appear to become refractory to mating for at least two days
after a primary courtship.

Courtship in Young Snails

Young Helix aspersa that have not yet grown a deflected
lip on the shell show courtship behavior like that of fully
adult snails, except that IDS behavior is not well devel-
oped, and snails in IDS tend to slide rather than press
their genitals against the body of the partner (10 of 12
snails, or 83%). These snails have mature ovotestes (2.e.,
they have sperm and mature oocytes), and they have pallial
gonoducts that appear to be mature in shape and nearly
of adult size. Some of these snails laid fertile eggs after
mating. This type of precocious mating has been observed
before in H. aspersa (COWIE, 1980) and in other stylom-
matophorans (BAuR, 1984).

Quantitative Analysis of Courtship Behavior
Related to Dart Shooting

Of the 34 pairs of snails in Figure 3A that went through
a primary courtship sequence, enough data were available
on 30 pairs to analyze (1) the timing of DS in courtship,
and (2) the effect of dart receipt on courtship behavior.
Seventeen of the 30 snails (28%) possessed no darts but
showed DS behavior. The histories of these snails were
unknown, and the possession of a dart by a snail before
DS was unknown to the observer. This natural difference
between snails allowed comparisons of courtship behavior
to be made between snails receiving darts and those not
receiving darts, in addition to the comparisons that could
be made between behaviors before and after DS in those
snails that received darts.

Page 31

n>
Oc
ee
ow
®
A
Sn
—
ep)
Se
o O
(Ss
Es
-

0 10 20 30 40 50 60

Timestor DiS fGminy)
Figure 4

Time between dart shootings (DS-1 and DS-2) vs. time from
start of courtship to the first dart shooting. Two groups were
pooled—pairs in which both partners possessed darts and pairs
in which only the second shooter possessed a dart—because the
regression lines for each of the two groups had slopes and
y-intercepts not significantly different from one another (P >
0.10, two-tailed ¢-tests). Both shooters with darts: Y = —0.036X
+ 13.575, r = —0.056 (nm = 15). Only second shooter with dart:
Y = —0.285X + 18.222, r = —0.300 (n = 10). Pooled data: Y =
—0.13% + 21.29, r = —0.186 (n = 25). In all three lines r is
not significantly different from zero (P > 0.10, two-tailed t-tests).

Data from the 30 pairs could be grouped according to
the relative order in which they went through DS and
whether or not they possessed a dart (see Table 1). The
data indicate that snails probably do not choose their part-
ners assortatively by possession of a dart, because there is
no significant difference between the observed and expected
numbers of pairs in which both snails possess darts (ob-
served, 15 pairs in which both snails possessed darts, vs.
expected, 16 pairs; P > 0.10, two-tailed binomial test).

Table 1 shows that the timing of DS during courtship
appears to vary greatly and appears to be affected by the
condition or age of the snail. The average time from the
beginning of courtship to DS in the first shooter varies
from 1 to 58 min, with a mean of 26 min. Table 1 shows
that in pairs formed of one partner without a dart and one
partner with a dart, snails lacking a dart are likely to go
through DS first (10 vs. 3 pairs; P < 0.05, one-tailed
binomial test; assuming a prior: p = q = 0.5). A pair-wise
comparison of the row marginals for the time to first DS
gives a similar result. There is a significant difference in
the time to first DS between snails without darts (16.8
min) and snails with darts (32.4 min) (P < 0.01, one-
tailed Wilcoxon two-sample test). A comparison of the
time to first DS between snails lacking darts and snails
possessing darts, both mated to partners with darts (the
first column on the left in Table 1), also shows that snails

Page 32

Table 1

Helix aspersa. Time to DS-1 from start of courtship. * +
SD; sample size in parentheses.

Second shooter

First shooter With dart Without dart Totals
With dart 344+13.7 227451 32.4 + 13.4
(15) (3) (18)
Without dart 458 == 11028) 2658S OF. 16.8 + 14.2
(10) (2) (12)
Totals 26.6 + 15.8 WNP se 5f3 POY ae 5.5
(25) (5) (30)

lacking darts go through DS sooner (14.8 min) than snails
possessing darts (34.4 min); (P < 0.01, one-tailed Wil-
coxon two-sample test). This last result is essentially equiv-
alent to the test on the row marginals, because the condition
of the second shooter appears to make no difference on the
time to DS in the first shooter (P > 0.05, two-tailed Wil-
coxon two-sample tests on the upper row—34.4 vs. 22.7
min—and column marginals—26.6 vs. 24.2 min). Com-
parisons involving the data on the two pairs where both
partners lacked darts cannot be made, owing to the small
sample size of this group.

The time that the second shooter took to go through DS
after its partner went through DS is shown in Table 2. A
comparison of the column marginals (17.4 vs. 22.8 min)
in Table 2 shows that the condition of the second shooter
(possession or non-possession of a dart) does not appear
to affect the timing of DS in the second shooter (P > 0.05,
two-tailed Wilcoxon two-sample test). However, compar-
ison of the two cells of the upper row of Table 2 indicates
that snails without darts are significantly slower to go
through DS (27.3 min) than snails with darts (16.5 min)
(P < 0.025, one-tailed Wilcoxon two-sample test). These
results indicate that snails without darts are perhaps more
easily injured or slowed down by dart receipt than snails
with darts.

As shown in Table 2, there is no synchrony in DS
between the two partners; second shooters take an average
of 19 min (range: 4-41 min) to go through DS after the
partner has gone through DS. Also, a plot of the time
between the first and second DS versus the time to the
first DS for the 25 pairs in which the second shooter
possessed a dart (Figure 4) shows no correlation between
the two variables (P > 0.05, two-tailed t-test of Hy: slope =
0). These results indicate that courting snails tend to space
their DS behavior apart, although the data do not indicate
what cues the snails use to achieve this. Receipt of a dart
does not appear to be the cause of the spacing of DS,
because the regression line for the group in which the
second shooter received a dart (first shooter possessed a
dart) appears to be coincident with the regression line for

The Veliger, Vol. 30, No. 1

Table 2

Helix aspersa. Time between DS-1 and DS-2. « + SD;
sample size in parentheses.

Second shooter

First shooter With dart Without dart Totals
With dart 16.5 22 10.7/ Dia 32 IP3) 18.3 + 11.4
(15) (3) (18)
Without dart ID) se iil GOES 19.2 + 11.0
(10) (2) (12)
Totals 17.4 + 11.4 Ap f a5 i72,il NGo7 se ilil2
(25) (5) (30)

pairs in which the second shooter received no dart (first
shooter lacked a dart) (two-tailed t-tests for equal slopes
and Y-intercepts, P > 0.05).

The data in Table 2 can also be used to test the effect
that dart receipt has on subsequent courtship behavior,
because the time between the first and second DS can be
used as a measure of how quickly the second shooter makes
the transition to the copulation phase after the partner has
gone through DS. A comparison of the row marginals in
Table 2 shows that snails receiving a dart do not take a
significantly shorter time to make the transition to the
copulation phase than snails not receiving a dart (18.3 min
vs. 19.2 min, respectively; P > 0.05, two-tailed Wilcoxon
two-sample test). The same result is obtained when com-
paring the cells on the left in Table 2 (second shooter with
a dart, first shooter with or without a dart) (16.5 min vs.
19.9 min; P > 0.05, two-tailed Wilcoxon two-sample test).

The effect of dart receipt was examined on three other
measures of courtship behavior: (1) rate of biting, (2) frac-
tion of time spent away from genital contact (FTC), and
(3) rate of AC. Data were most complete for pairs in which
the second shooter possessed a dart, and tests for the effect
of dart receipt on courtship were performed only on this
group (equivalent to the two cells of the column on the
left in Table 1). Two types of tests were performed. The
first type of test was a comparison of the behavior of snails
receiving a dart versus snails not receiving a dart—z.e., the
behavior in the group where the first shooter had a dart
versus the group where the first shooter lacked a dart. The
second type of test, performed on the same variables, was
a comparison between the behavior of snails before and
after receiving a dart, in the group where both snails pos-
sessed darts.

In addition to these tests on dart receipt, the effect of
dart shooting on a snail’s behavior was examined. The rate
of biting and the fraction of time spent out of genital contact
(FTC) were each compared for the first shooter before
and after it went through DS, in the group where both
snails possessed darts.

The variables were defined as follows.

ID), Jfs ID), Cintas, O37

(1) Biting rate:

# bites initiated by
snail from beginning
of LG-1 to DS-1

= 1G

(a) before partner went _

through DS Tyetore receipt before receipt

# bites initiated
by snail between

(b) after partner went _ DS-1 and DS-2
= Ste

through DS T

afler receipt after receipt

Both (a) and (b) calculated for the second shooter.

# bites initiated by
snail from beginning

(c) before going e of LG-1 to DS-1

through DS Liner shooting TCrcfore shooting
# bites initiated
by snail between
(d) after going sss DS-1 and DS-2
through DS AU ten shooting ra Tyner shooting

Both (c) and (d) calculated only for the first shooter.

(2) Fraction of time spent out of genital contact (FTC):

AN Gh apne
(a) before partner went through DS = Se
before receipt
Crea
(b) after partner went through DS = ir wt

afler receipt

Both (a) and (b) calculated for the second shooter.

INC :
(c) before going through DS = aaa e ae batons shooting
before shooting
WCrer ;
(d) after going through DS = T ate
after shooting

Both (c) and (d) calculated only for the first shooter.
(3) Rate of AC:

# of AC from
(a) before partner went _ DS-1 to DS-2

through DS ~ time from DS-1
to DS-2 (min)
# of AC from
(b) after partner went — DS-2 toC
through DS ~ time from DS-2
to C (min)

Both (a) and (b) calculated for the first shooter, and (b)
also calculated for the second shooter.

T = total time the second shooter spent in
dart shooting phase before partner went
through DS (time from beginning of
LG-1 to DS-1, in min)

before receipt

Page 33

T = total time the second shooter spent in
dart shooting phase after partner went
through DS (time from DS-1 to DS-2,
in min)

Toetore shooting = total time the first shooter spent in dart
shooting phase before it went through
DS (time from beginning of LG-1 to
DS-1, in min)

Titer shooin, = total time the first shooter spent in cop-
ulation phase after going through DS
and before being darted by its partner
(time from DS-1 to DS-2, in min)

os ipl ami wel craretenoounes a lvatte receipt. fletcrenoctne

TC ap = time from LG-1 to DS-1 spent in I +

TF + P that the second shooter initiated
(min)

T Carer recip = time from DS-1 to DS-2 spent in I +
TF + P that the second shooter initiated
(min)

TC gefore shootine = time from beginning of LG-1 to DS-1
spentinI + TF + P that the first shooter
initiated (min)

TG per shooine = time from DS-1 to DS-2 spent in I +

TF + P that the first shooter initiated
(min)

DS-1 = first DS, DS-2 = second DS. LG-1 begins for both
partners at the same time.

A comparison of snails that received a dart with snails
that received no dart shows that there are no significant
differences in the means for biting rate and FTC between
these two groups (Table 3A). Similar tests for the effect
of dart receipt (Table 3B) shows that there are no sig-
nificant differences in the mean biting rate and mean FTC
before and after dart receipt. However, a signed ranks test
for equal variances shows that the variance in biting rate
is greater in snails that received a dart than in snails that
received no dart (Table 3A). There is no statistically sig-
nificant difference in the variances of snails receiving and
snails not receiving a dart in FTC (Table 3A). These
results suggest that dart receipt has no influence on FTC
but that dart receipt (or a behavioral change associated
with DS in one or both of the partners) has an effect on
the biting rate. Dart receipt appears to cause a heteroge-
neous change in the rate of biting—an increase in biting
rate in a few snails and a decrease in others, so that the
variance in the biting rate increases.

Tests of the effect of dart receipt on the rate of AC
(Table 4) yielded results that appear contradictory. Snails
receiving a dart have a significantly lower rate of AC than
those not receiving a dart (Table 4A; for second shooters).
However, the rate of AC after dart receipt is significantly
higher after than before dart receipt in first shooters (Table
4B). The differences in the results may possibly be ex-
plained by the differences in the two types of tests. Probably
the best intepretation of the results is that dart receipt
causes a decrease in the rate of AC and that the IDS

aller receipt

Page 34

Table 3

Helix aspersa. Effect of dart receipt on biting rate and FTC.
x + SD; n = sample size.

A. Snails receiving a dart (the first snail to receive a dart in pairs
in which both snails have darts) vs. snails not receiving a dart
(partner did not possess a dart).

Received dart Received no dart

Biting rate! 0.24 + 0.52 0.02 + 0.04
n= 15 n= 10

FTC? 0.30 + 0.25 0.14 + 0.19
n= 15 n= 10

B. Before vs. after dart receipt in pairs where both partners
possessed darts.

Before receipt After receipt

Biting rate? 0.08 + 0.06 0.33 + 0.60
n= 11 n= 11

FTC 0.17 + 0.12 0.30 + 0.25
n= 15 n= 15

' Variances, but not means, significantly different. P > 0.10,
one-tailed Wilcoxon two-sample test for means; P < 0.001, one-
tailed squared ranks test for equal variances.

? Variances and means not significantly different. P > 0.10,
two-tailed Wilcoxon two-sample test for means; P > 0.05, one-
tailed squared ranks test for equal variances.

> Difference between means not significantly different. P >
0.10, two-tailed Wilcoxon test for paired observations.

* Difference between means not significantly different. P >
0.10, two-tailed Wilcoxon test for paired observations.

behavior of the partner depresses the rate of AC in a snail
to a possibly greater degree than that caused by dart re-
ceipt. The snails in Table 4A interacted with a partner
that had already passed into the copulation phase and was
also attempting copulation. In contrast, the snails in Table
4B that had not yet received a dart were interacting with
partners in IDS; and it was observed in this study that
IDS behavior in a snail frequently made it difficult for a
partner to court. If IDS in a snail suppresses the rate of
AC in a partner, then the rate of AC in the partner may
increase after the snail has gone through DS, in spite of
the partner’s receipt of a dart wound.

By comparison to the mostly negative effects of dart
receipt on the courtship behavior of the receiver, dart shoot-
ing has a pronounced effect on the shooter. It has already
been noted that penial eversion and attempted copulation
never occurs before dart shooting in snails going through
primary courtship. Another behavioral change appears to
be a decrease in the rate of biting after dart shooting (Table
5). FTC appears to be unaffected by dart shooting (Table
5).

DISCUSSION

Major differences in courtship behavior between Helix
aspersa and H. pomatia are seen in the courtship positions

The Veliger, Vol. 30, No. 1

Table 4

Helix aspersa. Effect of dart receipt on rate of AC. Rate:

x + SD; n = sample size.

A. Snails receiving a dart vs. snails not receiving a dart.!
Received dart Received no dart
0.53 + 0.17 0.83 + 0.23
n= 13 n=8
B. Before vs. after receiving a dart.’
Before receipt

0.47 + 0.63
n= 13

After receipt

0.56 + 0.21
n= 13

'Means, but not variances, significantly different. P < 0.05,
two-tailed Wilcoxon two-sample test for equal means; P > 0.10,
two-tailed squared ranks test for equal variances.

* Differences between means significantly different. P < 0.05,
two-tailed Wilcoxon test for paired observations.

used to maintain physical contact and in the method of
spermatophore transfer. To maintain physical contact,
courting individuals of H. pomatia lift the anterior region
of the soles off the substrate and press them together, while
courting H. aspersa remain with their soles on the substrate
and press their genitals together. Copulation in H. pomatia
is of brief duration (spermatophores expelled in 4.5 min;
intromission lasting 5.6 min), and part of the spermato-
phore is deposited external to the genital opening (LIND,
1973, 1976), whereas in H. aspersa virtually the entire
spermatophore is transferred directly into the partner’s
genitals over a period of an hour or more towards the end
of an intromission that lasts 6 h or longer.

A comparison of the overall courtship sequences of Helix
aspersa and H. pomatia shows that major aspects of dart
shooting behavior are similar in both species. The inte-
gration of DS behavior in the courtship sequence of H.
aspersa is like that of H. pomatia in that (1) the possession
of an immature dart is always accompanied by a secondary
courtship sequence, (2) DS behavior is never omitted (z.e.,
is not a conditional behavior) in a primary courtship se-
quence, and (3) AC never takes place in primary courtship
until after a snail has gone through DS. In both species
the courtship sequence is fairly rigid, and the type of court-
ship sequence that a snail goes through is strictly associated
with the contents of its dart sac and not with the condition
of the partner.

In addition to the association of the type of courtship
sequence with the contents of the dart sac, there is an
association between the absence of a dart in a snail going
through DS and the prior sexual history of the snail.
CHUNG (1986b) found that virgin Helix aspersa lack
darts (an hypothesis proposed in the last century by
BOUCHARD-CHANTEREAUX, 1839) and that at least 95%
of the virgin snails start growing darts after going through
an initial DS. (All fully adult, non-virgin H. aspersa possess

D. J. D. Chung, 1987

Page 35

Table 5

Helix aspersa. Effect of dart shooting on rate of biting and
FTC on snails that shot their dart first. « + SD; n =
sample size.

Before shooting After shooting n
Biting rate! 0.11 + 0.08 0.05 + 0.07 11
FTC 0.18 + 0.10 0.19 + 0.23 15

' Means significantly different. P < 0.05, two-tailed Wilcoxon
test for paired observations.

* Means not significantly different. P > 0.10, two-tailed Wil-
coxon test for paired observations.

darts.) Thus, a snail going through DS but not possessing
a dart is likely to be a young snail.

Because the presence or absence of DS and the posses-
sion or lack of a dart during DS behavior reflect the re-
productive condition of the shooter, a snail might be able
to assess the physical condition of a partner by the presence
or absence of DS behavior or a dart in the partner. For
instance, receipt or non-receipt of a dart might be used by
a snail to decide on whether or not to continue with court-
ship and copulation. However, there is little evidence from
either the courtship sequences (Figure 3) or the quanti-
tative tests that this occurs. In only one of 34 pairs going
through a primary courtship sequence did a snail withdraw
from courtship after its partner went through DS (its part-
ner had no dart); and snails receiving darts appear to be
more likely to reduce their rate of attempted copulation
rather than increase it (Table 4). The decrease in the rate
of AC in snails receiving darts indicate that snails are
physically hurt by dart receipt.

DS is unlikely to be used by a shooter to test the vigor
or readiness of a partner, because (1) snails appear to be
harmed by dart receipt and (2) none of the snails that
withdrew from courtship withdrew after receiving a dart.
It is unlikely on theoretical grounds that DS is used by a
shooter to test the vigor of a partner, because there is a
prolonged period of courtship that takes place before dart
shooting in which snails can assess one another. Dart
shooting is also unlike a final act in an escalated aggressive
display, because dart shooting is not a conditional behavior
in the courtship of snails that possess a fully formed dart.

The results of the quantitative tests on dart shooting in
Helix aspersa are similar to the resutls of tests on H. pomatia
(LIND, 1976; JEPPESEN, 1976) in that they show that dart
receipt apparently has no obvious stimulatory effect on
snails of either species. LIND (1976) tested the following
hypotheses on the effect of dart receipt: (1) receipt was a
prerequisite for carrying through copulation, (2) receipt
caused an immediate increase in the intensity of mating
activity, (3) receipt caused a decrease in the latency of
mating activity after dart receipt, and (4) receipt sped
subsequent pre-copulatory behavior. Lind could not prove
any of the hypotheses. The first hypothesis was rejected

by both Lind and Jeppesen and is also rejected in this
paper, because both H. pomatia and H. aspersa that have
shot darts will attempt copulation whether or not they
receive darts. Thus, dart receipt in these two species does
not act to trigger copulatory behavior and does not appear
to signal a snail’s vigor to its partner. The tests of the
effect of dart receipt on the rate of AC and on FTC reported
here are essentially tests of Lind’s second hypothesis, and
the results of the tests (Tables 3, 4) do not support this
hypothesis.

GODDARD (1962) believed that the injury to the body
caused by dart receipt in Helix aspersa stimulated an “in-
jury discharge” from the nervous system that subsequently
induced penial activity at the time of copulation. His hy-
pothesis appears to be incorrect, as this study and LIND’s
(1976) study show that dart receipt does not cause penial
eversion.

The test of the effect of dart receipt on the biting rate
reported here is, in part, a test of WEBB’s (1952b) hy-
pothesis that darts are used to stimulate courtship and also
prevent a partner from biting the shooter’s genitals. Webb’s
hypothesis could not be verified. The test on biting rate
(Table 3) appears to indicate that dart receipt causes some
snails to decrease their rate of biting and others to increase
their biting rate, although the average rate does not change
significantly. The cause of this heterogeneity in response
is unknown but may be due to an underlying heterogeneity
in the vigor or reproductive condition of darted snails.

The effect of dart receipt may possibly be delayed until
after courtship, or the dart may influence the physiology
of the snail. ToMPA (1980, 1984) suggested that the effect
of dart receipt may be to stimulate maturation and release
of ova in a recipient snail, and thereby increase the chances
of fertilization of eggs by the dart-shooting snail. This
hypothesis has not been tested directly. DORELLO’s (1925)
and BORNCHEN’s (1967) hypothesis that darts are used to
convey stimulatory substances from the mucous gland se-
cretions into the circulation of a darted snail suggests that
the primary effect of dart receipt may be a physiological
change that may not greatly affect specific courtship be-
haviors.

The hypothesis that darts are used to inoculate a snail
with bioactive mucous gland secretions was tested by CHUNG
(1986a). Injection of mucous gland extract into non-courting
snails caused genital eversions similar to those seen in
courting snails; topical application of the extract had no
effect on the behavior of assayed snails. The results of the
study suggested that the bioactive substance in the mucous
glands (possibly a peptide) stimulates the simultaneous
relaxation of the muscles of the terminal genitals and con-
traction of the body wall musculature to cause genital
eversion. No great changes in genital eversion were seen
in courting Helix aspersa that received a dart in this study
and none were noted in the studies of LIND (1976) and
JEPPESEN (1976) on H. pomatia. This might be explained
by the fact that courting snails almost always have a full

Page 36

genital eversion at the time of dart receipt, and any further
change in the condition of the genitals after dart receipt
cannot be detected easily in behavioral observations.

The courtship observations made on Helix aspersa and
observations made on other dart-bearing land snails sug-
gest two possible effects of dart receipt that are inconsistent
with the physical stimulation hypothesis (as defined by
GODDARD, 1962, and by LIND, 1976) but are not incon-
sistent with the chemical stimulation hypothesis (as de-
veloped by CHUNG, 1986a). Dart receipt may (1) cause a
snail to slow its movements and remain quiescent during
the copulation phase of courtship, or (2) affect the func-
tioning of the penis.

The Helix aspersa observed in this study appeared to
crawl more slowly after receiving a dart, although the
average crawling speed could not be quantified. The slow-
ing of movement may be due to the physical injury of dart
receipt; however, mucous gland secretions might possibly
affect the muscles used for crawling. WEBB (1952b) sug-
gested from courtship observations that dart receipt in
helminthoglyptids prevent premature withdrawal during
transmission of the spermatophore. However, this hy-
pothesis has never been tested.

Darting of the penis has been observed in a few species
and may be a function of the dart in some species. The
fusion of the male and female tracts near the genital ap-
erture in stylommatophorans would appear to allow the
dart to be shot into the everted genitals of mating partners;
and the anatomical placement of the dart sac on the vagina
in many species of dart-bearing snails would appear to
allow the darting of the penis during copulation. The penis
is almost never darted in Helix aspersa, and darts are al-
ways shot before intromission in this species, but darting
of the penis might occur regularly in Philomycus caroli-
nianus and species of Ventridens. WEBB (1968a) reported
that the dart in Philomycus injures the partner’s penis
during copulation. The dart is also reported to pierce the
everted penis, along with other organs, during courtship
and copulation in Ventridens (WEBB, 1968b). Whether the
non-deciduous dart in Philomycus and Ventridens is used
to impair the functioning of the male organs or is used as
a kind of holdfast was not determined by Webb. In this
study, only one H. aspersa (about 1% of more than 100
snails observed) received a dart in its everted penis; this
snail could not achieve intromission and copulated as a
“female” (allowing intromission and accepting a sper-
matophore but not secreting a spermatophore). This un-
usual case cannot be regarded as normal, but the suppres-
sion of male functioning by the dart in this case is interesting.
The dart in H. aspersa and other helicids cannot be used
as a holdfast, because it is deciduous.

The morphology and anatomical placement of the dart
indicate that the darts in most dart-bearing species with
non-deciduous darts do not function as purely physical
holdfasts, in the way that penial hooks function. None of
the published observations of dart shooting behavior clearly

The Veliger, Vol. 30, No. 1

shows a dart being used as a holdfast, although the thin,
curved dart of Ventridens might theoretically be able phys-
ically to restrain a partner. KUNKEL’s (1929, 1933) hy-
pothesis that the hollow, perforated dart of Vitrina elongata
is used as a suction cup for holding onto the shell of the
partner seems unlikely. Kunkel did not demonstrate how
effective suction could be applied from a dart tip that has
a diameter of 0.078 to 0.094 mm, on a partner about 1
cm long; and no one has demonstrated a suction mechanism
in the dart apparatus of Vitrina elongata or in any other
dart-bearing species.

Adaptive Significance of the Dart Apparatus

Observations on the courtship behavior of Helix aspersa
and other dart-bearing snails have not been able to deter-
mine the adaptive significance and evolution of dart-shoot-
ing behavior, but the data from this and other studies
indicate that the dart apparatus may have arisen in the
context of sexual selection in simultaneous hermaphro-
dites. There are three general evolutionary models that
could account for the evolution of the dart apparatus: (1)
the reproductive isolation model, (2) the courtship co-or-
dination model, and (3) the sexual selection model. The
data on dart-shooting and reproductive behavior in dart-
bearing snails are most consistent with the sexual selection
model, least consistent with the courtship co-ordination
model, and do not provide any support for the reproductive
isolation model.

Both Diver (1940) and WEBB (1952b) assumed that
the dart was used in species recognition during courtship
and evolved in this context. However, this hypothesis has
never been tested, and appears unlikely on theoretical
grounds. Helix aspersa, H. pomatia, and other dart-bearing
snails go through a fairly prolonged period of introductory
courtship behavior (with physical contact) before they show
dart-shooting behavior. This would argue against the use
of the dart as a species recognition device, because both
physical cues (e.g., the differences in courtship postures
between H. aspersa and H. pomatia) and probable chemical
cues are capable of being passed during the introductory
phase before dart shooting. The physical stimulus of dart
penetration may not be an ideal signal in species recog-
nition, because the degree and location of dart penetration
vary greatly (LIND, 1976; this study). The transfer of a
chemical signal used in species recognition by the dart may
be an evolutionarily suboptimal strategy, because (1) dart
receipt harms a potential mating partner and (2) sexual
pheromones, including contact pheromones used in court-
ship, are usually among the first signals transferred in
courtship.

WeBB (1951) noted a single instance of heterospecific
courtship between two species of dart-bearing Helmin-
thoglypta, where one of the snails died four days after
receiving a dart wound during courtship. This is the only
observation suggesting that the dart might be used in species

D. J. D. Chung, 1987

recognition; however, no evidence obtained since Webb’s
observation has supported his contention that the dart
evolved as a species-recognition device.

In the courtship co-ordination model, the behavior of a
courting partner is assumed to be an adaptation for pro-
moting co-operative exchange and use of gametes. It is in
the context of this model that LIND (1976) implicitly de-
fined the “stimulatory” action of the dart of Helix pomatia,
and it was in this context that the “stimulation” hypothesis
was defined in this paper. The lack of evidence for the
stimulation hypothesis, as defined by the courtship co-
ordination model, for both H. pomatia and H. aspersa in-
dicates that the dart is not used to aid co-ordination in
courtship. Dart receipt, in fact, appears to cause physical
harm: H. pomatia is less likely to complete courtship when
darted (LIND, 1976), and H. aspersa appears to reduce the
rate of penial eversion when darted. Dart shooting, by
contrast, appears to facilitate the completion of courtship
by the shooter: H. pomatia and H. aspersa attempt copu-
lation only after going through DS in primary courtship,
and H. aspersa reduces the rate of biting after shooting its
dart. Thus, it is the shooter and not the receiver of the
dart that appears to be “stimulated” by DS behavior.

Evidence for the evolution of species-specific genital
structures through sexual selection is growing (see reviews
by WEsT-EBERHARD, 1983; EBERHARD, 1985), and species-
specific dart morphologies likely reflect sexual selection
rather than selection for prezygotic reproductive isolating
mechanisms. The data showing that the shooter and not
the receiver is stimulated by DS behavior and that the
receiver is hurt by dart receipt suggests that there is an
evolutionary conflict of interest between the mating part-
ners, similar to that between the males and females of
gonochoristic species. Because the variance in male repro-
ductive success is usually greater than variance in female
reproductive success (see BLUM & BLUM, 1979; WILLSON
& BURLEY, 1983), under certain conditions simultaneous
hermaphrodites that act as “males” (those transferring
sperm but not using received sperm) may be favored over
those acting as pure hermaphrodites. The form of sexual
selection occurring in these simultaneous hermaphroditic
snails might be of two forms: (1) “cheating” by male-
acting hermaphrodites and the use of anti-cheating devices
by pure hermaphrodites, and (2) the use of coercion by
male-acting hermaphrodites to force partners to behave as
a “female.” Cheating (acting as a “male,” by transferring
sperm but not accepting or using received sperm) and the
use of anti-cheating strategies have been hypothesized to
occur in the hamlet Hypoplectrus (FISCHER, 1981, 1984).
In this fish, cheating may have given rise to a counter
strategy, or anti-cheating strategy, known as egg trading,
in which mating partners alternate male and female roles
several times in a single spawning bout. Sperm trading in
the opisthobranch Navanax (LEONARD & LUKOWIAK, 1984)
may have evolved under similar sexual selection pressures.
In the other form of sexual selection in hermaphrodites,

Page 37

coercive tactics in courtship and mating (e.g., incapacitating
a partner’s male organs, or forcefully stimulating the fe-
male organs to receptivity) can be simultaneously used
offensively and defensively. These two forms of sexual
selection are theoretically similar, although cheating does
not necessarily involve any type of coercion of the mates.
The dart may have arisen either as an anti-cheating mech-
anism or as a device used in coercion. The dart may have
evolved from smaller penial stylets or genital hooks in a
kind of evolutionary arms escalation that allowed the evo-
lution of increasingly larger or more effective darts to force
the partner to act as a “female.” Any destabilizing effect
of strong sexual selection on the hermaphroditic condition
(see CHARNOV, 1979, 1982) might be reduced by energy
recouped from allosperm digested in the gametolytic organs
found in pulmonates and many opisthobranchs.

Because dart receipt appears to be harmful to a snail,
it does not seem likely that darts evolved through runaway
sexual selection by female choice on stimulatory male gen-
ital structures (as suggested by EBERHARD, 1985, for darts
and other elaborate genitalia). The commonly made as-
sumption that darts (and other spicular genital structures
in animals) act to stimulate co-operative mating behavior
by mating partners may have to be re-examined.

By comparison with work done on the male accessory
gland secretions in insects (see GILLOT & FRIEDEL, 1977;
CHEN, 1984), mucous gland pheromones of Helix might
affect: (1) potentiation of sperm, (2) induction of egg mat-
uration or oviposition (TOMPA, 1980), and (3) the reduc-
tion of subsequent receptivity in mating partners (reduc-
tion of subsequent “female” receptivity). The possession
of separate sperm-digestion and allosperm-storing organs
in pulmonates and many opisthobranchs suggest several
other theoretical functions of dart receipt, including (1)
suppression of allosperm digestion, (2) displacement of
previously stored allosperm, or (3) prevention of subse-
quent allosperm storage. Of these possible effects, a re-
duction of subsequent mating seems to be unlikely in H.
aspersa, because snails will mate repeatedly with different
partners in a single breeding season in the laboratory (per-
sonal observations). The other hypotheses have not been
tested directly. The consideration of these and other evo-
lutionary hypotheses may prove to be as profitable to the
study of molluscan reproductive biology as they have been
to studies on other groups of animals (e.g., see BLUM &
BLuM, 1979).

ACKNOWLEDGMENTS

I am deeply indebted to Alex Tompa for sharing with me
his considerable expertise on malacology and darts. I thank
James Cather, Norman Kemp, and Brian Hazlett for of-
fering important and useful suggestions on this study.
Richard Alexander and Joel Weichsel were helpful in
discussing with me various hypotheses on the evolution of
the dart apparatus. Finally, I must thank William Ham-

Page 38

ilton for pointing out the cheating/anti-cheating hypoth-
esis and providing early encouragement to me. This study
was financed in part by grants from the University of
Michigan and the Hawaiian Malacological Society.

LITERATURE CITED

Baur, B. 1984. Early maturity and breeding in Arianta arbus-
torum (L.) (Pulmonata: Helicidae). Jour. Moll. Stud. 50:
241-242.

Bium, M.S. & N. A. BLUM. 1979. Sexual selection and re-
productive competition in insects. Academic Press: New York.
463 pp.

BORNCHEN, M. 1967. Untersuchungen zur Sekretion der fin-
gerformigen Drusen von Helix pomatia. Z. Zellforsch. Mik-
rosk. Anat. 78:402-426.

BOUCHARD-CHANTEREAUX, N. R. 1839. Observations sur les
moeurs de divers Mollusques terrestres et fluviatiles observés
dans le département du Pas-de-Calais. Ann. Sci. Natur.
(Zool.) 11:295-307.

CHARNOV, E. L. 1979. Simultaneous hermaphroditism and
sexual selection. Proc. Natl. Acad. Sci. 76:2480-2484.
Cuarnov, E. L. 1982. The theory of sex allocation. Monogr.

Pop. Biol. 18:1-355.

CHEN, P.S. 1984. The functional morphology and biochemistry
of insect male accessory glands and their secretions. Ann.
Rev. Entomol. 29:233-255.

CHUNG, D. 1986a. Stimulation of genital eversion in the land
snail Helix aspersa by extracts of the glands of the dart
apparatus. Jour. Exp. Zool. 238:129-139.

CHuNG, D. 1986b. Initiation of growth of the first dart in Helix
aspersa Muller. Jour. Moll. Stud. 52:253-255.

Conover, W. J. 1980. Practical nonparametric statistics. 2nd
ed. John Wiley & Sons: New York. 493 pp.

Cowlkg, R.H. 1980. Precocious breeding of Theba pisana (Miul-
ler) (Pulmonata: Helicidae). Jour. Conch. 30:238.

DasEN, D. D. 1933. Structure and function of the reproductive
system in Ariophanta ligulata. Proc. Zool. Soc. (1933):97-
118.

DILLAMAN, R. M. 1981. Dart formation in Helix aspersa.
Zoomorphology 97:247-261.

Diver, C. 1940. The problem of closely-related species living
in the same area. Pp. 303-328. In: J. S. Huxley (ed.), The
new systematics. Clarendon Press: Oxford.

DORELLO, P. 1925. Sulla funzione della glandole digitate nel
gen. Helix. Atti della reale academia nazionale dei lincei,
Ser. 6, Rendiconti, Classe di scienze fisiche, matematiche e
naturali 1:47-51.

EBERHARD, W.G. 1985. Sexual selection and animal genitalia.
Harvard University Press: Cambridge, Mass. 244 pp.
FIscHER, E. A. 1981. Sexual allocation in a simultaneously
hermaphroditic coral reef fish. Amer. Natur. 117:64-82.
FIscHER, E. A. 1984. Local mate competition and sex allocation
in simultaneous hermaphrodites. Amer. Natur. 124:590-

596.

ForcarT, L. 1949. Die Erektion der Kopulationsorgane und
der Kopulationsmodus von Phenacolimax major (Fér.). Arch.
Moll. 77:115-119.

GERHARDT, U. 1935. Weitere Untersuchung zur Kopulation
der Nacktschnecken. A. Morphol. Oekol. Tiere 30:297-332.

GittoTT, C. & T. FRIEDEL. 1977. Fecundity-enhancing and
receptivity-inhibiting substances produced by male insects:
a review. Adv. Invert. Reprod. 1:199-218.

GiusTI, F. & A. Lepri. 1980. Aspetti morphologici ed etologici

The Veliger, Vol. 30, No. 1

dell’accoppiamento in alcune specie della famiglia Helicidae
(Gastropoda, Pulmonata). Atti Accademia Fisiocritici Siena
(1980):11-71.

GoppDarRD, C. K. 1962. Function of the penial apparatus of
Helix aspersa. Australian Jour. Biol. Sci. 15:218-232.
HERZBERG, F. & A. HERZBERG. 1962. Observations on repro-

duction in Helix aspersa. Amer. Natur. 68:297-306.

JEPPESEN, L. L. 1976. The control of mating behaviour in
Helix pomatia L. (Gastropoda: Pulmonata). Anim. Behav.
24:275-290.

KUNKEL, K. 1928. Zur Biologie von Eulota fruticum Muller.
Zool. Jahr. Jena (Abt. f. allg. Zool. u. Physiol.) 45:317-
342.

KUNKEL, K. 1929. Experimentelle Studie Uber Vitrina brevis
Ferussac. Zool. Jahrb. Jena (Abt. f. allg. Zool. u. Physiol.)
45:575-626.

KUNKEL, K. 1933. Vergleichende experimentelle Studie uber
Vitrina elongata Draparnaud und Vitrina brevis Ferussac.
Zool. Jahr. Jena (Abt. f. allg. Zool. u. Physiol.) 52:399-
432.

LEONARD, J. L. & K. Lukowiak. 1984. Male-female conflict
in a simultaneous hermaphrodite resolved by sperm trading.
Amer. Natur. 124:282-286.

Linp, H. 1973. The functional significance of the spermato-
phore and the fate of spermatozoa in the genital tract of
Helix pomatia (Gastropoda: Stylommatophora). Jour. Zool.
(Lond.) 169:39-64.

LinD, H. 1976. Causal and functional organization of the mat-
ing behaviour sequence in Helix pomatia (Pulmonata, Gas-
tropoda). Behaviour 59:162-202.

MEISENHEIMER, J. 1912. Die Weinbergschnecke Helix pomatia.
Leipzig. 140 pp.

PruvoT-FoL, A. 1960. Les organes génitaux des opistho-
branches. Arch. Zool. Exp. et Gen. 99:135-224.

Raut, S. K. & K. C. GHOSE. 1984. Pestiferous land snails of
India. Zool. Survey India, Tech. Monogr. No. 11.

RENSCH, I. 1955. On some Indian land snails. Jour. Bombay
Natur. Hist. Soc. 53:163-176.

SoKAL, R.R. & F. J. ROHLF. 1969. Biometry. W. H. Freeman
& Co.: San Francisco. 776 pp.

Tompa, A. 1980. The ultrastructure and mineralogy of the
dart from Philomycus carolinianus with a brief survey of the
occurrence of darts in land snails. Veliger 23:35-42.

Tompa, A. 1982. X-ray radiographic examination of dart for-
mation in Helix aspersa. Netherlands Jour. Zool. 32:63-71.

Tompa, A. 1984. Land snails. Pp. 48-140. In: A. Tompa, N.
H. Verdonk & J. A. M. van den Biggelaar (eds.), The
Mollusca, Vol. 7, Reproduction. Academic Press: New York.

vaN Mot, J. J. 1970. Revision des Urocyclidae (Mollusca,
Gastropoda, Pulmonata). Ann. Mus. Roy. de]’Afrique Centr.,
Tervuren, No. 180.

WEBB, G. R. 1942. Comparative observations of the mating
habits of three California land snails. Bull. So. Calif. Acad.
Sci. 41:102-108.

Wess, G. R. 1948. Notes on the mating of some Zonztoides
(Ventridens) species. of land snails. Amer. Mid]. Natur. 40:
435-461.

Wess, G. R. 1951. An instance of amixia between two species
of landsnails. Amer. Natur. 85:137-139.

Wess, G. R. 1952a. Pulmonata, Xanthonycidae: comparative
sexological studies of the North American land-snail, Mon-
adenia fidelis—a seeming ally of Mexican helicoids. Gastro-
podia 1:1-3.

Wess, G. R. 1952b. Pulmonata: Helminthoglyptidae: sexo-
logical data on the landsnails Cepolis maynard: and Hel-

Dee Da Chungy 198i

minthoglypta traski field: and their evolutionary significance.
Gastropodia 1:4-5.

Wess, G.R. 1968a. Observations on the sexology of Philomycus
carolinianus (Bosc.). Gastropodia 1:62.

WesB, G. R. 1968b. Sexological notes on Ventridens elliotti, V.
acerra, V. demissus britts:, and V. ligera. Gastropodia 1:67-
70.

Page 39

Wess, G. R. 1980. The sexology of a Texan Humboldtiana.
Gastropodia 2:2-7.

WEST-EBERHARD, M. J. 1983. Sexual selection, social com-
petition, and speciation. Quart. Rev. Biol. 58:155-183.
WILLSON, M. F. & N. BuRLEY. 1983. Mate choice in plants:
tactics, mechanisms, and consequences. Monogr. Pop. Biol.

19:1-251.

The Veliger 30(1):40-45 (July 1, 1987)

THE VELIGER
© CMS, Inc., 1987

Ecology and Burrowing Behavior of Ascobulla ulla

(Opisthobranchia: Ascoglossa)

DUANE E. DE FREESE

Department of Biological Sciences, Florida Institute of Technology,
Melbourne, Florida 32901, U.S.A.

Abstract. A population of Ascobulla ulla, a tectibranch ascoglossan (=sacoglossan), was sampled on
a high-energy jetty environment at Fort Pierce Inlet, Florida. The highest densities of A. u//a occurred
during warm summer months when the surf was calm and the alga Caulerpa racemosa was more abundant.
The habitat requirements for A. u//a appear to be narrow, resulting in seasonal fluctuations in population
size. The ability to burrow in the more protected microhabitats where C. racemosa occurs is an important
specialization that also adapts A. ulla for life in its high-energy habitat. The unusual burrowing behavior
of A. ulla, involving the bilobed cephalic shield and a rotational twisting and periodic flexion of the thin
shell, is described from field and laboratory observations.

INTRODUCTION

Ascobulla, Volvatella, and Cylindrobulla represent a phy-
logenetic link between the burrowing cephalaspidiform
opisthobranchs and the more advanced epifaunal tecti-
branch Ascoglossa (THOMPSON, 1979; CLARK, 1982). In-
formation about Ascobulla ulla has been limited to taxo-
nomic descriptions (MaRcus & Marcus, 1956, 1970;
Marcus, 1972) and some brief ecological observations
(CLARK & JENSEN, 1981; JENSEN & CLARK, 1983). As-
cobulla ulla has been reported from “muddy algae” at the
Enseada of Guaruja, east of Santos, Brazil (MARCUS &
Marcus, 1956); in association with mangroves at Key
Biscayne, Florida (MARCUS, 1972); on the rhizoids of the
alga Caulerpa paspaloides (Bory) Grev. at Key Largo, Flor-
ida (JENSEN & CLARK, 1983); in association with man-
groves at Twin Cays, Belize, Central America (Clark and
De Freese, unpublished data); and on the rhizoids of C.
racemosa (Forsskal) J. Ag. at Crawl Key, Florida (personal
observation) and at Fort Pierce Inlet, Florida (JENSEN &
CLARK, 1983).

The inlet at Fort Pierce represents the northernmost
record for Ascobulla ulla and is close to the northern limits
of the tropical siphonalean algal community (JENSEN &
CLARK, 1983). Although high-energy habitats are often
overlooked as suitable collecting sites for ascoglossans, 13
ascoglossan species have been collected from this habitat
type (JENSEN & CLARK, 1983). The aim of this paper is
to describe aspects of the behavior and population biology
of A. ulla, emphasizing the burrowing behavior, habitat

selection, and effects of environmental stress on the pop-
ulation at Fort Pierce Inlet, Florida.

STATION DESCRIPTION

Fort Pierce Inlet (27°28'N, 80°18'W) connects the Indian
River Lagoon system to Florida’s Atlantic Coast (Figure
1). The inlet is defined by two man-made rock jetties that
extend into the Atlantic Ocean. Ascobulla ulla predomi-
nantly inhabits the tidepools and the leeward side of boul-
ders along the north face of the north jetty and is associated
with algal mats of Caulerpa racemosa. These microenvi-
ronments are often subjected to severe wave disturbance,
especially during late summer and fall (tropical distur-
bances) and during the winter (northern cold fronts). The
inlet is also affected by upwelling events that occur each
summer along the east coast of Florida (GREEN, 1944;
SMITH, 1982).

MATERIALS anp METHODS

The population of Ascobulla ulla at Fort Pierce Inlet was
sampled monthly from May 1984 to September 1985. Ini-
tially, samples were taken along two transects parallel to
the jetty. One transect was positioned along the northern
edge of the jetty where the rocks outcrop on the sandy
beach. This transect included Caulerpa racemosa patches.
The other transect, established 2 m to the north, was
located in an area of bare sand only. Ascobulla ulla occurred
only in association with C. racemosa. This alga was re-

D. E. De Freese, 1987

Florida

Page 41

Atlantic
Ocean

Figure |

Location of the sampling site at Ft. Pierce Inlet, Florida. Site indicated by asterisk.

stricted to hard substrata and the areas of sand adjacent
to boulders of the jetty. All subsequent samples were taken
at sites having 100% algal cover. Because optimal habitats
were chosen for sampling sites, the population density data
are presented as “maximal density” (.e., the highest an-
imal densities found for each monthly sampling date).
Samples were taken using a 10-cm diameter PVC corer
inserted to an approximate depth of 10 cm. Deeper cores
(20 cm) were taken between December 1984 and March
1985, in an attempt to locate A. ulla. Sample sites were
categorized as upper intertidal, midtidal, or subtidal hab-
itats. Samples were washed through a 0.5-mm sieve and
sorted in the field. Animals were transported live to the
laboratory in 2-L plastic bottles containing seawater.

A midsummer (1985) sediment sample was collected
from a site adjacent to the jetty where Ascobulla ulla was
abundant. This sample was analyzed for particle size com-
position (median particle size = 0.22 mm, 2.2 o) (Went-
worth classification). Based upon graphical analysis
(BUCHANAN & Kain, 1971) the sediment was poorly sorted
(a, = 1.23), coarse skewed (SK, = 0.11), and mesokurtic
(K, = 1.10). For consistency, this sediment sample was
used for all burrowing trials.

Burrowing time was measured at 10, 15, 20, 26, and
30°C. Animals were allowed to adjust at experimental
temperatures for approximately 30 min in fingerbowls
containing seawater. After 30 min the animals were trans-
ferred to a fingerbowl containing the midsummer (1985)

sediment sample and seawater maintained at the experi-
mental temperature. The “digging period,” defined as the
time elapsed between the first probing by the foot and the
complete coverage of the shell by sand (TRUEMAN &
ANSELL, 1969), was measured with a stopwatch.

Burrowing behavior was observed in narrow, glass
aquaria containing sediment and seawater. The mecha-
nism of burrowing was recorded with a video camera and
video cassette recorder (VCR). Ascobulla ulla was carefully
placed on the substratum at the glass-sediment interface.
Burrowing activity began immediately and often proceeded
along this interface, enabling detailed observations of sub-
surface behavior.

RESULTS
Distribution and Abundance

Densities of Ascobulla ulla were generally low (Figure
2) except for population peaks during May (1984 and
1985), which coincided with the presence of stable stands
of Caulerpa racemosa. Animal lengths and densities fluc-
tuated during the summer months. In July 1984, the pop-
ulations of both A. ulla and C. racemosa appeared to decline
with lower temperatures accompanying an apparent up-
welling event, and by August both populations were sig-
nificantly reduced.

Most individuals of Ascobulla ulla were collected in the
sediment layer associated with the algal mat. The sediment

The Veliger, Vol. 30, No. 1

Page 42

om» on GOH GOGH Oo
oo tT FH OANA er

(ww) HISNS1 114SHS NVA

YM

LLL
TLL

LLL
WM
YM

YM
HWM

w) w)
BeBe

(_3HO9 "‘N) ALISN3G TVWIXVW

on on +t ON TO

TIME (MONTHS)

D. E. De Freese, 1987

LATERAL VIEW

HEAD INSERTION :
SHELL = MASS ANCHOR .
SHELL ORIENTATION

TERMINAL ANCHOR

Page 43

DORSAL VIEW

SHELL RETRACTION
CEPHALIC SHIELD FLARE

EXTENSION

Figure 3

The mechanism of burrowing in Ascobulla ulla. Sequence from lateral and dorsal views.

that accumulated along the leeward rock faces rarely ex-
ceeded 1 cm in depth. Ascobulla ulla was usually in direct
contact with the rhizoids of Caulerpa racemosa (0-3 cm
depth). Animals were also collected in the sand surround-
ing anchored clumps of C. racemosa in protected tidepools.
Under these protected conditions, A. ulla occasionally
emerged from the sediment and crawled up the assimilators
of the alga for egg deposition and feeding. This behavior
has also been observed in the laboratory and at other field
collection sites (Belize, Central America; Crawl Key, Flor-
ida Keys).

Maximal animal size and density occurred during the
warm summer months, when surf conditions were gen-
erally calm. Caulerpa racemosa was most abundant along
the shallow areas of the jetty. In deeper water (2-3 m),
well-developed stands of another alga, Halimeda discoidea
(Decaisne), predominated, and C. racemosa was uncommon
at these depths. A decrease in the C. racemosa population
was observed after upwelling events, coastal storms, and
heavy rainfall. During the fall and winter months, no
specimens of Ascobulla ulla were collected, and C. racemosa
was observed only occasionally.

The Mechanism of Burrowing

The mechanism of burrowing in Ascobulla ulla is illus-
trated in Figure 3, and described using the burrowing
terminology of TRUEMAN & ANSELL (1969).

When Ascobulla ulla is placed on the sandy substratum,
the animal begins burrowing almost immediately and con-

tinues until it is completely buried. Burrowing is initiated
by the insertion of the propodium and the anterior end of
the bilobed cephalic shield into the substratum. At this
stage, the shell functions as a mass anchor, enabling the
anterior end to take on a vermiform shape, which probes
and wedges into the substratum. This penetration phase
is accompanied by slight side-to-side movement. After the
head is inserted into the substratum, it functions as a
terminal anchor, facilitating shell orientation and increas-
ing the angle of penetration. During the shell-orientation
phase, the head and propodium continue to extend deeper
into the sediment. As the shell approaches a vertical po-
sition in relation to the substratum, the cephalic shield
flares, laterally compresses the sediment, and thus firmly
establishes the terminal anchor. The shell is then slowly
pulled into the substratum until it contacts the median
furrow at the posterior end of the cephalic shield. Shell
insertion is accompanied by the rhythmic pumping and
rotational twisting of the shell as it “augers in.” The shell
apex bears a spiral slit that physically separates the whorls
(Marcus & Marcus, 1956), thus permitting the periodic
contraction and expansion of the shell. This allows the
shell to function as a penetration anchor during the ex-
pansion phase (when mantle musculature relaxes), and
presents minimal cross-sectional area during retraction
(terminal anchoring by head). When observed from the
apical view, the shell appears as a spring that coils
and uncoils. The rotational twisting of the shell has not
been reported for other infaunal opisthobranchs and ap-
pears to facilitate shell retraction. The animal repeats this

Figure 2

Composite figure of seasonal data taken at Ft. Pierce Inlet. Mean Shell Length: ® = mean; vertical lines = standard
deviation. Caulerpa Coverage Index (*CCI): 0 = no Caulerpa, 1 = sparse coverage, 2 = short growth + clumped
distribution, 3 = well-developed growth + clumped distribution, 4 = well-developed growth + broad coverage, 5 =
dense growth + broad coverage. Temperature: ® = water temperature in °C. Maximal Animal Density: A = upper

intertidal zone, O = midtidal zone, 0 = subtidal zone.

Page 44

(sec)

BURROWING TIME

2 3 4 5 6
SHELL LENGTH (mm)
Figure 4

Rate of burrowing versus shell length of Ascobulla ulla, at three
temperatures. @ = 20°C: (Y = 36.86% — 56.80, r = 0.9659, n =
5). & = 26°C: (Y = 11.45X + 28.65, 7 = 0.7912, n = 7). B=
30°C: (Y = 16.43X% + 5.25, r = 0.7462, n = 10).

sequence of penetration, shell orientation, head extension,
cephalic shield flare, and shell retraction until burial is
complete. Mucus secreted at the anterior end of the shell
appears to prevent the movement of substratum particles
into the mantle cavity. Slight disturbances such as water
currents or rough handling resulted in a rapid, copious
discharge of dilute, milky white mucus from the posterior
region of the shell. Animals anchor to the algae or sediment
by viscous mucous threads zn situ if exposed during wave
surge.

Burrowing Rate

Figure 4 shows the effects of animal size and water
temperature on the burial rate of Ascobulla ulla. At 10°C,
A. ulla was immobilized; no movements or attempts at
burrowing were observed. At 15°C, the experimental an-
imals slowly twisted their head and attempted to probe
the substratum. After 10 minutes, several animals had
achieved head penetration, although burial was clearly
impaired. At 20, 26, and 30°C, burrowing time generally
increased with increasing animal size.

DISCUSSION

Peak population densities of Ascobulla ulla coincide with
the presence of well-developed mats of the alga Caulerpa

The Veliger, Vol. 30, No. 1

racemosa, their specific food source. Reductions in the pop-
ulation of A. ulla appear to coincide with thermal stress,
rainfall-induced salinity changes, and high-energy surf
conditions. The great magnitude of these population re-
ductions suggests that climatic variations in the high-en-
ergy intertidal zone heavily constrain populations of A. ulla
and such high-energy areas appear to represent a marginal
habitat.

In Elysia tuca Marcus, 1967, an epifaunal ascoglossan
that feeds on Halimeda spp., seasonal climatic factors ap-
pear to affect several parameters, including the retention
of functional plastids, egg deposition, feeding rate, and
growth rate (WAUGH & CLARK, 1986). The biotic and
abiotic constraints on ascoglossan populations are not fully
understood, providing a fertile area for additional research.

A variety of environmental factors appear to have im-
portant effects on the stability of the Caulerpa racemosa
population. Changes in the quality or quantity of the food
alga may have a direct effect on the animal population
owing to the stenophagous nature of Ascobulla ulla. The
algal population appears to decline at lower temperatures
associated with summer upwelling events. In addition, C.
racemosa may be adversely affected by high summer tem-
peratures, which often exceeded 30°C in the shallow in-
tertidal pools. This was especially evident when low tides
prevented an open exchange of seawater.

The apparent disappearance of Ascobulla ulla during the
fall and winter months coincides with a seasonal transition
to rougher surf conditions, increased turbidity, and de-
creasing water temperatures. The effects of these factors
and others, such as photoperiod and irradiance, are not
known. Ascobulla ulla appears to be capable of maintaining
its position on the assimilators of the alga in a moving
current or a light surge, but the animals are easily displaced
from the alga by moderate shaking of the thallus, which
indicates a vulnerability to high surf or heavy surge con-
ditions during emergence. Ascobulla ulla may also emerge
at high tide, when depth could provide some protection
from surface waves. Ascobulla ulla may burrow more deeply
into the sediment during fall and winter. Although deeper
core samples were taken during the winter months when
A. ulla was uncommon or absent, no evidence was found
to confirm this hypothesis. Ascobulla ulla has direct devel-
opment (CLARK & JENSEN, 1981); therefore, a winter bur-
rowing response or undiscovered, subtidal, winter habitats
could account for the rapid spring colonization observed
at the sampling site. The disappearance of A. ulla from
the jetty habitat during the winter suggests that vernal
recolonization occurs from deep-water populations inhab-
iting reefs adjacent to the jetty. Direct development pre-
sents some advantages to the colonization of high-energy
beaches because juveniles are presumably able to burrow
immediately and faster if juvenile size approximates sed-
iment grain size, and the efficient recruitment associated
with direct development should enable a rapid increase in
the population. The coincidence of low tides and freezing
temperatures observed during the winter of 1985 might

D. E. De Freese, 1987

also explain the slow rate of vegetative recolonization of
Caulerpa racemosa in the intertidal areas.

The habitat requirements for Ascobulla ulla appear to
be quite narrow, resulting in seasonal fluctuations in pop-
ulation stability. Data on population dynamics, zoogeo-
graphic distribution, and the effects of temperature on
burrowing rates support a hypothesis that A. ulla is rel-
atively stenothermal. Because Fort Pierce represents the
distributional limit of several tropical and subtropical as-
coglossan and siphonalean species (JENSEN & CLARK,
1983), minor climatological conditions may have important
effects on floral and faunal distributions.

The bilobed cephalic shield characteristic of Ascobulla
ulla enhances the burrowing capability of this primitive
ascoglossan and may function as a more efficient terminal
anchor than the single broad cephalic shield of most prim-
itive infaunal cephalaspids. The distinctive apical spiral
slit of the thin shell permits cross-sectional changes that
may aid the flow of water through the mantle cavity as
well as provide a more efficient penetration anchor during
burrowing. Contraction and passive relaxation of the shell
adductor muscle control the rhythmic pumping of the shell
(Marcus & Marcus, 1956). A detailed analysis of mus-
cular structure, similar to BRACE’s (1977) anatomical study
of some tectibranch opisthobranchs, would further clarify
the burrowing mechanics of A. ulla.

The burrowing sequence in Ascobulla ulla diverges from
the behavior of the cephalaspid Haminea antillarum (d’Or-
bigny, 1842). Haminea antillarum has a single broad ce-
phalic shield, which is used to plow slowly into the sedi-
ment at a shallow angle of penetration (TRUEMAN &
ANSELL, 1969; De Freese, personal observations).

Ascobulla ulla shares some similarities with the oxynoa-
cean Volvatella laguncula (Sowerby, 1894), which also ex-
hibits adduction movements of its flexible shell (THOMPSON,
1979). Because there was no obvious exclusion of partic-
ulate matter, THOMPSON (1979) suggested that V. lagun-
cula pumped a suspension of fine sediment through its
mantle cavity. An alternate hypothesis, by CLARK (1982),
suggests that shell adduction in V. laguncula may assist
burrowing in compacted sand, by loosening the sediment
surrounding the shell, and coincidentally increasing the
availability of interstitial water for respiratory needs.

Ascobulla ulla burrows at considerably slower rates than
more typical, infaunal, high-energy beach organisms: Mac-
tra olorina burrows in 1.5 sec (ANSELL & TREVALLION,
1969) and the burrowing rate of Donax denticulatus de-
clines from 2.9 sec at 32°C to 8.15 sec at 24°C (TRUEMAN,
1983).

Data on burrowing rates, habitat preference, and sea-
sonal population stability suggest that Ascobulla ulla should
not be strictly viewed as a high-energy beach organism.
However, burrowing is an important capability that allows
A. ulla to exploit the high-energy habitat at Fort Pierce
Inlet, Florida.

Page 45

ACKNOWLEDGMENTS

Great appreciation is expressed to Kerry B. Clark for his
guidance, suggestions, and criticisms. I would also like to
thank R. L. Turner, W. G. Nelson, and two anonymous
reviewers for critically reviewing the manuscript. The work
was partly supported by the Lerner-Gray Fund for Ma-
rine Research of the American Museum of Natural His-
tory and by a Doctoral Dissertation Research Improve-
ment Grant OCE-8501715 from the National Science
Foundation.

LITERATURE CITED

ANSELL, A. D. & A. TREVALLION. 1969. Behavioral adaptations
of intertidal molluscs from a tropical sandy beach. Jour.
Exp. Mar. Biol. Ecol. 4:9-35.

Brace, R. C. 1977. The functional anatomy of the mantle
complex and columellar muscle of tectibranch molluscs (Gas-
tropoda: Opisthobranchia), and its bearing on the evolution
of opisthobranch organization. Phil. Trans. R. Soc. Lond.
B, 277:1-56.

BUCHANAN, J. B. & J. M. Kain. 1971. Measurement of the
physical and chemical environment. Pp. 30-58. In: N. A.
Holme and A. D. McIntyre (eds.), Methods for the study
of marine benthos. IBP Handbook No. 16. Blackwell Sci-
entific Publ.: Oxford.

Cxiark, K. B. 1982. A new Volvatella (Mollusca: Ascoglossa)
from Bermuda, with comments on the genus. Bull. Mar. Sci.
32(1):112-120.

CxiarK, K. B. & K. R. JENSEN. 1981. A comparison of egg
size, capsule size, and development patterns in the order
Ascoglossa (Sacoglossa) (Mollusca: Opisthobranchia). Int.
Jour. Invert. Reprod. 3:57-64.

GREEN, C. 1944. Summer upwelling—northeast coast of Flor-
ida. Science 100:546-547.

JENSEN, K. & K. B. CLark. 1983. Annotated checklist of Flor-
ida ascoglossan Opisthobranchia. Nautilus 94(1):1-13.
Marcus, E. 1972. On some opisthobranchs from Florida. Bull.

Mar. Sci. 22:284-308.

Marcus, E. & E. Marcus. 1956. On the tectibranch gastropod
Cylindrobulla. Anais Acad. Brasil. Ciéncias 28:119-128.
Marcus, E. & E. Marcus. 1970. Opisthobranchs from Cu-
racao and faunistically related regions. Stud. Fauna Curacao

33:1-129.

SMITH, N. P. 1982. Upwelling in Atlantic shelf waters of south
Florida. Florida Sci. 45(2):125-138.

THompson, T. E. 1979. Biology and relationships of the South
African sacoglossan mollusc Volvatella laguncula. Jour. Zool.
(Lond.) 189:339-347.

TRUEMAN, E. R. 1983. Observations of the responses of the
tropical surf clam Donax denticulatus to changes of temper-
ature and salinity. Jour. Moll. Stud. 49:242-243.

TRUEMAN, E. R. & A. D. ANSELL. 1969. The mechanisms of
burrowing into soft substrata by marine animals. Oceanogr.
Mar. Biol. Ann. Review 7:315-366.

WauGu, G. R. & K. B. CLARK. 1986. Seasonal and geographic
variation in chlorophyll content of Elys:a tuca (Ascoglossa:
Opisthobranchia). Mar. Biol. 92:483-487.

The Veliger 30(1):46-54 (July 1, 1987)

THE VELIGER
© CMS, Inc., 1987

Cryptomya californica (Conrad, 1837): Observations on

Its Habitat, Behavior, Anatomy, and Physiology

EDWIN V. LAWRY

29681 Dane Lane, Junction City, Oregon 97448, U.S.A.

Abstract.

Descriptions and photographs of the estuarine habitat, external and internal structures,

and gut contents of the lamellibranch clam Cryptomya californica (Myoida: Myidae) are presented. Also
included are behavioral observations, and experimental information on the digestive tract and its as-

sociated bacteria.

INTRODUCTION

During my studies on spirochete bacteria of the genus
Cristispira (LAWRY, 1981; LAwRy et al., 1981), which are
isolated most frequently from the crystalline styles of var-
ious pelecypods and gastropods, few literature references
were found to my favorite source of spirochetes, the marine
clam Cryptomya californica (Conrad, 1837). However, the
importance of this small, burrowing lamellibranch in es-
tuarine ecosystems must be considerable, as it is a pre-
dominant animal in vast areas of mudflats along the Pacific
coast of America from Alaska to Peru (BROWN et al., 1977;
HERTLEIN & GRANT, 1972; KEEN, 1971; PETERSON, 1984;
WEST et al., 1976; WICKSTEN, 1978).

The majority of information available on Cryptomya
californica comes from a limited portion of its range (e.g.,
the central coast of California), and is contained in three
articles (MACGINITIE, 1934, 1935; YONGE, 1951). These
papers discuss the clam’s Monterey Bay habitats, its shell
morphology, anatomy, and particle filtering behavior, and
its unusual utilization of the tunnels of other burrowing
organisms. Curiously, almost nothing has been published
concerning the habitats of C. californica throughout the rest
of its range, its ecological niche, burrowing behavior, diges-
tive physiology, or reproduction.

In this paper, I compare Oregon estuarine habitats of
Cryptomya californica with those previously described in
California. The clam’s burrowing behavior is discussed,
and pre-existing anatomical data are reviewed, photo-
graphically documented, and embellished with new ob-
servations about the digestive tract, wandering amebocytes,
and gametes. The nature of the clam’s food and its pro-
cessing by the digestive system are investigated. Special
problems related to digestion are addressed, such as the
function of the crystalline style, how this organ is affected

by tidal rhythms, whether it contains digestive enzymes,
and, if so, whether they are of clam or bacterial origin.
Also discussed are other possible roles played by the clam’s
gut-associated bacteria.

MATERIALS anp METHODS

Cryptomya californica was collected from sandy mudflats
of Yaquina Bay and Coos Bay, Oregon. Photographic
records were made of the habitat, substrate, arrangement
of clams around the tunnels of the ghost shrimp Callianassa
californiensis (Dana, 1854) (see MACGINITIE, 1934), and
the burrowing behavior of the clam. In order to determine
the nature of the diet, intestinal contents and fecal pellets
were obtained from freshly collected clams.

To microscopically observe the internal anatomy of
Cryptomya californica, de-shelled, whole clams were fixed
and dehydrated using a freeze substitution technique. They
were then embedded in paraffin and cut into 7-wm thick
sections. These were stained with Harris’ hematoxylin and
eosin (H and E), and observed and photographed using a
Zeiss Universal microscope equipped with a Nikon AFM
automatic exposure meter and a 35 mm camera. Brightfield
optics were used to make photomicrographs of the digestive
organs. Phase contrast was used to demonstrate the pres-
ence of Cristispira within sections of the crystalline style.
Intestinal contents were photographed in situ using No-
marski optics.

A clam submerged in seawater was vivisected and pho-
tographed through a Nikon SMZ-10 zoom-lens dissecting
microscope in order to observe the digestive organs and
the direction and periodicity of crystalline style rotation,
which could be seen through the nearly transparent wall
of the style sac.

EK. V. Lawry, 1987

To observe the structure of the crystalline style (NELSON,
1918; YONGE, 1932), styles were extracted by making a
small incision into the stomach and forcing the style through
the opening by exerting light pressure onto the side of the
visceral mass. Each style was placed in a drop of seawater,
and phase contrast and Nomarski optics were used re-
spectively to photograph amebocytes on the outer surface
of the style (MATHERS, 1972; YONGE, 1926) and Cristispira
within the matrix. Sperm and eggs were collected during
vivisections and photographed in seawater using Nomarski
optics.

To determine whether populations of spirochetes in
Cryptomya californica are self-perpetuating, or whether they
dwindle after the clams are removed from their natural
habitat, the following test was performed. Changes in pop-
ulations of C7zstispira within the styles of clams held in
aquaria for several weeks were monitored by periodically
dissolving a known number of styles in an isotonic saline
solution (LAWRY ef al., 1981), measuring the total volume,
and counting all the spirochetes in 5-ul portions, using
darkfield microscopy. The average number of bacteria per
style was then calculated.

To gain further clues as to the roles of the crystalline
style in digestion, the possible presence of amylase, a starch-
hydrolyzing enzyme common in molluscan styles, was in-
vestigated (IORDACHESCU & DUMITRU, 1978; MATHERS,
1973). Styles were analyzed for amylase activity by placing
extracted styles, sterilized and washed with toluene, on
0.5% starch/marine nutrient agar culture medium (6 g
Sigma no. S-2630 soluble starch, 66 g Difco 2216 marine
nutrient agar, 1200 ml distilled water, autoclaved at 121°C
for 15 min) for 24 h at 20°C. Hydrolysis of the starch in
the medium was checked for by color-developing the plates
with Gram’s iodine.

To investigate whether gut-associated bacilli can pro-
duce amylase, possibly contributing to that stored in the
crystalline style, the following experiment was performed.
Colonies of Gram-negative, motile bacilli were isolated
from the surfaces of extracted, unsterilized styles streaked
on to the above-described medium. Their ability to hy-
drolyze starch was determined by subculturing the bacteria
to the same medium, incubating for 24 h at 20°C, and
color-developing the plates with Gram’s iodine.

The following observations were made to determine
whether the style is always present, or whether its presence
is affected by fluctuations in tides or food supplies, as in
some other intertidal mollusks (LANGTON, 1977; MATH-
ERS, 1974). The presence of styles in freshly collected clams
during low tides was noted. Clams removed from seawater
for 24 h at 10°C were checked for the presence of styles.
Cryptomya californica maintained (with food) in aerated
seawater (27 to 30%o salinity, 8°C) for extended periods
of time were examined for styles. The effects of 6 weeks
of starvation on style production were studied.

To observe the initial distribution of ingested particulate
matter within the digestive organs, carmine dye particles
(Allied Chemical Corp., National Aniline Div., Biological

Page 47

Stains Dept., cat. no. 475) were fed to clams. Other clams
were given the flagellated unicellular green alga Dunaliella
salina. The clams were dissected after 1 h, and the digestive
organs examined for the location of the ingested carmine
particles or algae.

RESULTS
Habitat

Cryptomya californica was easily found in sandy lower
estuarine mudflats of Yaquina Bay and Coos Bay, Oregon,
during tides lower than +0.3 m (Figure 1a). Individuals
were especially prevalent in areas inhabited by the ghost
shrimp Callianassa californiensis (Figures 1b, c). The clams
were usually embedded in the walls of the tunnels of the
shrimp (Figure 1d), with only their short siphons pro-
truding into the tunnels. This was sometimes difficult to
observe, as the tunnels tended to collapse during excava-
tion. Some specimens, however, were interred with no
obvious connection to a tunnel. Often hundreds of clams
were found in a square meter of substrate.

Burrowing Behavior

Clams placed on their side on submerged sand began to
burrow after a few minutes, if left undisturbed. Burrowing
takes place as follows. First, the siphons and large, ciliated
foot emerge (Figure 2a). The extended foot can assume
shapes ranging from knife-shaped to spade-shaped (Figure
3a), and muscular contractions, along with ciliary action
on the outer surface, enable the foot to dig rapidly into the
sand. The foot digs directly down into the sand, and when
it is firmly anchored, the animal pulls itself off its side
onto the anteroventral portion of the shell (Figure 2b). As
the foot continues to dig, the entire animal periodically
rocks in a dorsoventral plane, and with each rocking cycle
the animal works itself deeper into the substrate (Figure
2c). After about 5 min the entire clam, except for the
siphons, is completely buried (Figure 2d). Eventually the
organism burrows deeper into the sand. How far or fast
the clam can dig through the substrate, or how long it can
survive without reaching an adequate tunnel was not de-
termined in this study.

Anatomy

Shell morphology: The yellow-white, oblong shells are
fragile and small. Although specimens of Cryptomya cali-
fornica greater than 30 mm in length have been reported,
the majority of shells collected in this research were less
than 20 mm long. The shells gape at the posterior end,
and the right valve is slightly fuller than the left. Delicate
concentric growth lines are present. A brown periostracum
extends beyond the growing shell margin and protects the
mantle when it protrudes. The prominent chondrophore
(Figure 3b) protruding from the hinge of the left valve is
held by an internal resilium in the right valve (ABBOTT,

Page 48

The Veliger, Vol. 30, No. 1

Figure 1

The habitat of Cryptomya californica. a. A typical sandy estuarine mudflat, representative of the normal habitat of
C. californica. Coos Bay, Oregon. b. The usual appearance of the sandy substrate in which lives Cryptomya californica,
often in proximity to the tunnels of Callianassa californiensis. As seen from a height of 1.5 m. c. Callianassa califormensis
(female, 9 cm in length) burrowing into the sand. d. An excavation of a Callianassa burrow showing two Cryptomya
californica (arrows) with their short siphons oriented toward the tunnel. Found down to depths of 50 cm beneath
the surface of the sand, Cryptomya californica is usually 1 to 2 cm in length.

1974; HADERLIE & ABBOTT, 1980; QUAYLE, 1973; RUDY
& Ruby, 1983).

Siphons: The siphons, as described by YONGE (1951), are
extremely short (less than 1 mm in length). A membrane
controls the opening of the excurrent siphon, and a row

of tentacles protects the entrance of the incurrent siphon.
Both siphons are surrounded by an outer ring of tentacles.

Gills and palps: The relatively large gills (two demi-
branchs on either side of the body) are covered with cilia,
which rapidly pump water through the mantle cavity. The

E. V. Lawry, 1987

Page 49

Figure 2

The burrowing behavior of Cryptomya californica. a. A submerged C. californica lying on its right side, siphons and
foot extended. The foot begins to penetrate the sand. b. When the foot is anchored, the clam rights itself. c. The
clam rocks in a dorsoventral plane, and works itself into the substrate. In the gaping posterior portion of the shell
are the excurrent siphon (membrane closed) and the incurrent siphon, with its surrounding tentacles. Both are
encircled by an outer ring of tentacles. d. After about 5 min the clam is completely buried except for the siphons.

The scale in all four photographs is the same. Bar = 1 cm.

cilia also filter food particles from the water and concen-
trate them into streams of mucus, which are carried to the
mouth. Unusable particulate matter is sorted out by the
labial palps and condensed into pseudofeces, which are
transported by cilia posteriorly along the ventral portion
of the mantle, and periodically expelled through the in-
current siphon (YONGE, 1951).

Stomach and intestine: The esophagus and stomach are
surrounded by a large mass of digestive diverticula. The
intestine emerges from the right side of the stomach, and
I found its lumen to be connected for a short distance with
the lumen of the style sac. The intestine then winds ven-
trally toward the posterior portion of the foot, where it

loops dorsally to pass through the heart. The rectum runs
dorsally of the posterior adductor muscle, leading to the
anus just inside the excurrent siphon (YONGE, 1951).

Crystalline Style

A large style sac extends ventrally from the stomach
(Figures 3c, d). The style sac is nearly transparent and
has a seamlike structure, comprised of the major and minor
typhlosoles, along the length of the right side. I discovered
the ventral end of the style sac to be open to the body
cavity. Therefore, the organ is actually a tube rather than
a sac. The entire inner surface of the sac is lined with cilia,
which cause the crystalline style to rotate and to press its

Page 50 The Veliger, Vol. 30, No. 1

Figure 3

External and internal features of Cryptomya californica. a. Two specimens of C. californica, each with its muscular,
ciliated foot extended. The short siphons (arrows) are indicated at the posterior end of one clam. Bar = 1 cm. b.
Dorsal view of the valves of C. californica, with the chondrophore extending from the hinge of the left valve. The
ruler is marked in 1 mm intervals. c. Dissection of the digestive organs of C. californica, as seen from the left side.
The crystalline style, which is encased in a sac (arrow), protrudes into the stomach (S). Food is digested and
absorbed primarily in the digestive diverticula (D). The intestine (i) loops twice as it descends from the right side
of the stomach to an area near the ventral end of the style sac, where it curves dorsally (I) and carries waste
materials to the anus. These organs are surrounded by gonad. Bar = 2 mm. d; Photomicrograph of a section of the

E. V. Lawry, 1987

dorsal end against a prominent gastric shield in the stom-
ach.

The style of a vivisected clam submerged in seawater
was observed to rotate 7 to 30 rpm within its sac at water
temperatures from 10 to 21°C respectively. The speed in-
creased during several hours of observation, possibly owing
to a rise in water temperature or a loss of ciliary control.
The style rotated in a clockwise direction, the opposite
direction noted by YONGE (1951), as seen from the dorsal
end. I made these observations directly through the wall
of the intact style sac, as a grain of black sand was fixed
to the side of the style, and could be easily seen with each
rotation. Even after the style was removed, style sac ciliary
action continued for more than 5 h.

The crystalline style consists of a gelatinous, laminated
cortex and a liquid core. Mucoid material, apparently
being applied to or wound around the outer surface of the
style (as seen in the section in Figure 3e), appears to
originate from the intestine and, possibly, secretory cells
along the right side of the sac.

A crystalline style was always present in freshly col-
lected clams, those exposed to air for 24 h, those kept
submerged for long periods, and in clams that had been
starved for 6 weeks.

Spirochete bacteria of the genus Cristispira (Figure 4f)
were invariably found actively moving within the cortex
and core of the entire style (Figure 3f). They were also
observed in the stomach fluid, but not in the intestine or
rectum. Freshly collected clams contained thousands of
Cristispira. Although these bacteria appeared healthy and
active, and were observed to divide, their populations with-
in fed clams decreased steadily at rates of 5 to 12% per
day after clams were removed from their natural habitat.

Sterilized styles demonstrated amylase activity by hy-
drolyzing starch. Bacilli isolated from the surfaces of un-
sterilized styles also hydrolyzed starch.

Nutrition

The microscopic examination of intestinal contents (Fig-
ure 4a) and fecal pellets (Figure 4b) from freshly collected
clams showed that the animals normally ingest detritus
consisting mostly of diatoms and bacteria, but sometimes
containing dinoflagellates, crustacean and annelid setae,

Page 51

sand, and even pollen grains. The digestive diverticula of
fresh clams were usually green, presumably from chlo-
rophyll of ingested algae (MATHERS, 1972). Carmine par-
ticles fed to clams passed quickly through the stomach into
the intestine. No particles were observed in the digestive
diverticula or the style. Clams that had been fed Dunaliella
salina had algae (some still living) in the stomach 1 h after
feeding. Chlorophyll had been incorporated into the core
of the style in some cases.

Amebocytes

Rapidly moving amebocytes (Figure 4e) were often ob-
served on the outside of the anterior end of the crystalline
style. Such cells are elongate, measuring about 20 um in
length and 6 um in width. The round nucleus, 2.3 wm in
diameter, is centrally located. A large karyosome is in the
middle of the nucleus. The cytoplasm contains numerous
granules and vacuoles. These cells may be protozoan.

Gametes

The abundant gonads of Cryptomya californica, which
fill most of the visceral cavity, contain either sperm (Figure
4c) or eggs (Figure 4d). The acrosomes of sperm are 5 wm
long, tapered, and slightly curved. Including the flagellum,
sperm measure 45 wm in length. The mature eggs are
somewhat oblong, measuring 65 wm long and 53 wm at
the widest point. There is a round, eccentric nucleus which
is 30 um in diameter and contains a large, round, eccentric
nucleolus measuring 13 um across. The abundant cyto-
plasm contains numerous inclusions (DOHMEN, 1983;
LONGO, 1983; RAVEN, 1958).

DISCUSSION

Cryptomya californica occupies a nearly identical niche in
the Oregon estuaries studied as it does in Monterey Bay,
California. Dense populations of these clams are present
in large areas of marine bays and lower estuarine sandy
mudflats, especially in communities dominated by the ghost
shrimp Callianassa. Because of its short siphons, deeply
buried Cryptomya californica cannot have direct access to
the surface of the sand. The animals are, therefore, usually
embedded in the walls of tunnels of other burrowing or-

digestive organs lying immediately below the stomach (dorsal view). The crystalline style (C) is in a sac anterior
to the ascending intestine (I) and posterior to the digestive diverticula (D) and the esophagus (EF). At this level, the
descending intestine is connected along its left portion to the style sac. They separate at about 1 mm below the
stomach. The extensive lamellae (L) are also shown. H and E stain. Brightfield. Bar = 1 mm. e. Photomicrograph
of a cross section of the crystalline style and style sac. The style has a liquid core (C) and a laminated cortex (CX).
As seen from this dorsal view, the style rotates clockwise, propelled by the cilia of the columnar epithelial cells of
the sac. Style cortex material (arrow) seems to originate from the typhlosoles of the style sac. In this section, the
descending intestine (D) is connected to the style sac. H and E stain. Brightfield. Bar = 0.5 mm. f. Detail of the
style cortex from Figure 3e, showing the orientation of its contained spirochete bacteria, Cristispira. The arrow
indicates the outer edge of the style. Phase contrast. Bar = 0.1 mm.

Page 52 The Veliger, Vol. 30, No. 1

Figure 4

Cryptomya californica. a. A section through the descending intestine of a clam fixed immediately after collection,
showing ingested detritus, especially diatom fragments. H and E stain. Nomarski optics. Bar = 70 um. b. A portion
of a fecal pellet from a freshly collected clam. It contains the valves of diatoms and dinoflagellates, crustacean and

E. V. Lawry, 1987

ganisms such as the shrimps Callianassa californiensis and
Upogebia pugettensis, and (in California) the echiuran worm
Urechis caupo. The siphons protrude slightly into the tun-
nel, and the water therein is the source of oxygen and food,
and the depository for waste products.

The clams avoid predation and desiccation by living at
safe depths (down to 50 cm) within the sand, where they
undoubtedly take up residence early in their larval lives.
The collapsing of tunnels by tidal forces, the incessant
burrowing activities of Callianassa (MACGINITIE, 1934),
or the searching of humans for edible clams and ghost
shrimp for bait, may force Cryptomya californica to make
frequent moves. The large cilia-covered foot, which can
be extended through the pedal gape in the anteroventral
portion of the mantle, the small slim shell, and the unen-
cumbering siphons surely would facilitate movement
through the sandy substrate.

The stomach clearly plays an essential role in the partial
digestion and sorting of ingested substances (YONGE, 1923).
As a result of ciliary activity, rotation of the crystalline
style against the gastric shield, the release of enzymes from
the style and digestive diverticula, and possibly some bac-
terial digestive action, several digestive processes are ini-
tiated in the stomach. First, large particles, such as diatoms,
are shunted into the intestine, where degradation of con-
tained organic material may be facilitated by the action of
bacteria. Large numbers of motile bacilli were observed
in fresh fecal pellets, and I noted that they actively con-
gregated around masses of organic matter and diatoms
contained in the pellets. Second, lysis of some plant cells
takes place in the stomach. Third, much of the lysate and
probably considerable amounts of bacteria are directed into
the digestive diverticula to undergo further digestion and
absorption. Lastly, some of the partially digested food is
carried, along with quantities of mucus, into the style sac
to form the liquid core of the style. The substance forming
the laminated cortex of the style appears to be secreted by
cells of the intestine and the typhlosoles along the right
side of the style sac. While the core is continuously being
replenished in the stomach, the anterior portion of the
cortex is probably being dissolved there (MATHERS, 1974).
The significance of the opening in the ventral end of the
style sac is not clear. Some nutrient material may con-
ceivably pass directly from the style sac into the body cavity
through this aperture.

The crystalline style of Cryptomya californica is always
present regardless of prolonged periods of submergence or
exposure, or the presence or absence of food. Callianassa

Page 53

beds are normally exposed only during tides below +0.3
m, and during most low tides the shrimps’ tunnels probably
contain enough water to permit Cryptomya californica to
continue its respiratory and feeding activities (MAc-
GINITIE, 1934). The persistence of the style is likely an
adaptation to a nearly continuous feeding behavior.

MacGInitie (1934) felt that competition for food be-
tween Cryptomya californica and Upogebia or Urechis, both
of which are efficient plankton filterers, may explain why
the clam seems to be more plentiful in burrows of Calli-
anassa. The repiratory, burrowing, grooming, and sand-
filtering activities of Callianassa not only circulate food-
laden seawater through the burrow during high tides, but
also stir up detritus (mostly diatoms and bacteria) during
low tides. The alimentary canals of clams that I collected
were always full of detritus.

Cryptomya californica normally has thousands of Cris-
tispira in the stomach and matrix of the crystalline style.
It seems that this population of spirochetes must be con-
tinuously replenished by ingestion of bacteria from the
environment, as their numbers steadily decrease in clams
removed from their natural habitat, even though the size
of the styles does not decrease. The majority of the Crzs-
tispira are probably first incorporated into the core of the
style as mucus is drawn from the stomach into the style
sac. Afterwards, they make their way into the cortex, the
substance of which they are able to partially liquify. They
can be observed moving actively back and forth in liquid-
filled channels apparently of their own making. I have
observed these bacteria dividing 7m setu, but their growth
rate within the style probably cannot keep up with attri-
tion. Most are probably lost through the intestine, although
none were identified there in this study. The invariable
presence of a large, active population of spirochetes in the
styles of freshly collected clams suggests that the bacteria
may aid in the digestion of food materials ingested by the
host. Upon degradation, however, they may also serve as
a source of nutrition for the clam.

The crystalline style possesses the starch-hydrolyzing
enzyme amylase. The release of this enzyme in the stomach
assists in the digestion of plant materials normally con-
sumed by Cryptomya californica. Gram negative bacilli,
possibly Vibrio spp., which are always present in the stom-
ach and style sac, also produce starch-hydrolyzing en-
zymes. Thus, at least part of the enzyme found in the style
may be of bacterial origin. In my opinion, there is some
validity to each of the following hypotheses: (a) that the
crystalline style is an organ that stores digestive enzymes

annelid setae, plant material (including pollen grains), sand, and bacteria. Brightfield. Bar = 250 wm. c. Sperm of
C. californica. Nomarski optics. Bar = 20 um. d. An egg from C. californica, with its large round nucleus, prominent
nucleolus, and extensive cytoplasm. Nomarski optics. Bar = 30 um. e. Living, active amebocytes im situ on the outer
surface of the crystalline style. Numerous cytoplasmic inclusions are visible. Phase contrast. Bar = 20 um. f. Living
Cristispira sp. in situ within the matrix of the crystalline style. Nomarski optics. Bar = 20 um.

Page 54

needed during feeding, (b) that it is itself a site where some
digestion takes place, and (c) that some nutrients may be
stored within its matrix for subsequent use during periods
of food scarcity.

Amebocytes are often present on the outer surface of
the anterior half of a style taken from a fresh clam. These
cells are very active and contain numerous cytoplasmic
inclusions. If they are indeed of clam origin, which remains
to be shown, then presumably they act as scavengers main-
taining the style and style sac. They may transport nu-
trients to other portions of the body.

The majority of the body cavity is filled with gonad,
and immense numbers of sperm or eggs are produced.
Although I observed fecund specimens in May, no seasonal
data are available. Gametes are probably shed directly into
the tunnels of Callianassa and other mud-dwelling organ-
isms. The feeding activities of crustaceans, worms, mol-
lusks, and gobies within the tunnels no doubt contribute
greatly to the attrition of embryos and larvae (MACc-
GINITIE, 1934) of Cryptomya calvfornica.

ACKNOWLEDGMENTS

I thank John Baross, James Carlton, Carol Cogswell,
Daniel Gleason, Suzanne Hamilton, Harrison Howard,
Tena Lawry, Bayard McConnaughey, James McLean,
Norman McLean, Richard Morita, Sonja Rasmussen, Paul
and Lynn Rudy, and Donald Wimber for their kind as-
sistance during this research.

LITERATURE CITED

ABBOTT, R. T. 1974. American seashells: the marine Mollusca
of the Atlantic and Pacific coasts of North America. Van
Nostrand Reinhold Company: New York. 663 pp.

Brown, D. A., C. A. BAWDEN, K. W. CHATEL & T. R. PARSONS.
1977. The wildlife community of Iona Island jetty, Van-
couver, B.C., and heavy-metal pollution effects. Environ-
mental Conservation 4:213-2106.

DOHMEN, M. R. 1983. Gametogenesis. Pp. 1-48. In: K. M.
Wilbur, N. H. Verdonk & J. A. M. van den Biggelaar (eds.),
The Mollusca, Vol. 3: Development. Academic Press: New
York. 352 pp.

HADERLIE, E. C. & D. P. ABBoTT. 1980. Bivalvia: the clam
and allies. Pp. 355-411. In: R. H. Morris, D. P. Abbott &
E. C. Haderlie (eds.), Intertidal invertebrates of California.
Stanford University Press: Stanford, California. 690 pp.

HERTLEIN, L. G. & U. S. Grant. 1972. The geology and
paleontology of the marine Pliocene of San Diego, California.
Paleontology: Pelecypoda. San Diego Society of Natural
History, Memoir 2(Part 2B):135-409.

IORDACHESCU, D. & I. F. Dumitru. 1978. Some physiochem-
ical properties of a-amylase purified from the marine mollusc
Mya arenaria. Revue Roumaine de Biochimie 15:279-285.

KEEN, A.M. 1971. Sea shells of tropical West America: marine
molluscs form Baja California to Peru. Stanford University
Press: Stanford, California. 1064 pp.

The Veliger, Vol. 30, No. 1

LANGTON, R.W. 1977. Digestive rhythms in the mussel Mytilus
edulis. Mar. Biol. 41:53-58.

Lawry, E. V. 1981. The fine structure of Cristispira from the
lamellibranch Cryptomya californica Conrad. M.S. Thesis,
University of Oregon. 49 pp.

Lawry, E. V., H. M. Howarp, J. A. BARoss & R. Y. MoriTa.
1981. The fine structure of Cristispira from the lamelli-
branch Cryptomya californica Conrad. Cur. Microbiol. 6:355-
360.

LONGO, F. J. 1983. Meiotic maturation and fertilization. Pp.
49-89. In: K. M. Wilbur, N. H. Verdonk & J. A. M. van
den Biggelaar (eds.). The Mollusca, Vol. 3: Development.
Academic Press: New York. 352 pp.

MacGinitTig, G. E. 1934. The natural history of Callianassa
californiensis Dana. Amer. Midl. Natur. 15:166-177.

MacainitTig, G. E. 1935. Ecological aspects of a California
marine estuary. Amer. Midl. Natur. 16:629-765.

MatTHerS, N. F. 1972. The tracing of a natural algal food
labelled with a carbon 14 isotope through the digestive tract
of Ostrea edulis L. Proc. Malacol. Soc. Lond. 40:115-124.

MatTHuHers, N. F. 1973. A comparative histochemical survey of
enzymes associated with the processes of digestion in Ostrea
edulis and Crassostrea angulata (Mollusca: Bivalvia). Jour.
Zool. (Lond.) 169:169-179.

MatTHers, N. F. 1974. Digestion and pH variation in two
species of oysters. Proc. Malacol. Soc. Lond. 41:37-40.
NeELson, T. C. 1918. On the origin, nature, and function of
the crystalline style of lamellibranchs. Jour. Morphol. 31:

53-111.

PETERSON, C. H. 1984. Does a rigorous criterion for environ-
mental identity preclude the existence of multiple stable
points? Amer. Natur. 124:127-133.

QuayYLE, D. B. 1973. The intertidal bivalves of British Colum-
bia. British Columbia Provincial Museum: Victoria, B.C.
Handbook No. 17:104 pp.

RAVEN, C. P. 1958. Morphogenesis: the analysis of molluscan
development. Pergamon Press: New York. 311 pp.

Rupy, P. & L.H. Rupy. 1983. Oregon estuarine invertebrates:
an illustrated guide to the common and important inverte-
brate animals. Fish & Wildl. Serv., U.S. Dept. Inter.: Wash-
ington, D.C. 225 pp.

WEsT, R. R., P. C. Twiss, J. E. MATHEWSON & R. S. SWAIN.
1976. Some intertidal infauna and their substrate: Puerto
Penasco, Sonora. Trans. Kansas Acad. Sci. 79:113.

WICKSTEN, M.K. 1978. Checklist of marine mollusks at Coyote
Point Park, San Francisco Bay, California. Veliger 21:127-
130.

YONGE, C.M. 1923. The mechanism of feeding, digestion, and
assimilation in the lamellibranch Mya. Jour. Exper. Biol. 1:
15-63.

YONGE, C. M. 1926. Structure and physiology of the organs
of feeding and digestion in Ostrea edulis. Jour. Mar. Biol.
Assoc. U.K. 14:295-386.

YONGE, C. M. 1932. The crystalline style of the Mollusca.
Science Progress 26:643-653.

YONGE, C. M. 1951. Studies on Pacific coast mollusks: I. On
the structure and adaptations of Cryptomya californica Con-
rad. Univ. California Publ. Zool. 55:395-400.

The Veliger 30(1):55-68 (July 1, 1987)

THE VELIGER
© CMS, Inc., 1987

Gametogenesis and Reproductive Cycle of the Surf
Clam Mesodesma donacium (Lamarck, 1818)
(Bivalvia: Mesodesmatidae) at
Queule Beach, Southern Chile

by

SANTIAGO PEREDO, ESPERANZA PARADA, anp IVAN VALDEBENITO

Department of Biology, Catholic University of Chile-Temuco,
Casilla 15-D, Temuco, Chile

Abstract.

The gonadal organization, cytological characteristics of gametogenesis, and reproductive

cycle in the surf clam Mesodesma donacium, from Queule Beach, southern Chile, were studied histo-
logically using light microscopy. Monthly analysis of the proportion of sexes revealed a sex ratio of 1:1.
In both sexes, gonads are ramified organs bearing numerous follicles closely packed among coils of the
intestine. Gametogenesis follows the general plan described in most marine bivalves. Gametes at different
stages of maturation can be recognized by their shape, size, and nuclear features in both sexes. The
reproductive cycle is annual, with a maturation period from June through November (winter and
spring). Spawning extends from December to April (summer and early autumn), peaking in December
and January. Gonads undergo a short recovery period during May and then start a new cycle.

INTRODUCTION

The reproductive cycles of mollusks of commercial value
inhabiting Chile’s extensive coastline have been described
from a variety of locations on the coast. Among the la-
mellibranch bivalves are Aulacomya ater (LOZADA, 1968;
SoOLis & LozapA, 1971), Choromytilus chorus (LOZADA et
al., 1971; PEREZ-OLEA, 1981), Ostrea chilensis (WALNE,
1963; SOLis, 1967) and Venus antiqua (LOZADA & BUSTOS,
1984). These studies, in addition to furnishing reproduc-
tive data that have allowed an adequate management of
these species, have also shown variations in the timing of
gametogenesis and spawning in populations from different
geographical areas. These latitudinal variations are ascribed
to environmental factors that present local variations and
exert exogenous control on reproduction. Among these fac-
tors, the most relevant are temperature and abundance of
food (GIESE & PEARSE, 1977).

The reproductive cvcle of the surf clam Mesodesma do-
nacium has been studied by BROWN & GUERRA (1979) in
Guanaqueros (30°15’S, 71°41’W) and TARIFENO (1980)
at the Laguna Beach area of Valparaiso (32°30'S, 71°30'W).
These studies have shown differences in the timing of
gametogenesis and spa.vning period in the populations

studied. The present study describes the sex ratio, game-
togenesis, and seasonal gonadal changes of a surf clam
population from Queule Beach (39°25'S, 73°13'W). This
locality was selected as the study area because it has po-
tential for commercial operations and the area appears to

contain a large population of the surf clam.

MATERIALS anp METHODS

Monthly samples of surf clams were collected from a bed
in the mid-littoral level of Queule Beach (39°25’S, 73°13’W)
from August 1983 to November 1984. Each sample con-
sisted of 230 clams. From these samples, 15 males and 15
females in the shell length range of 61 to 75 mm were
selected for histological study. This size range was chosen
to avoid inclusion of juvenile surf clams (sexually immature
individuals). The viscera were fixed in aqueous Bouin’s
fixative. After embedding in paraffin, 7-um serial sections
were cut and stained with hematoxylin and eosin. Ten to
15 sections through different regions of the gonads of each
specimen were examined under the light microscope to
determine the gonadal organization, the cytological char-
acteristics of gametogenesis, and the seasonal gametogenic

cycle.

Page 56

%o

75

50

25

1983

The Veliger, Vol. 30, No. 1

1984

Figure 1

Proportions of females and males in the Mesodesma donacium population from Queule Beach.

The remaining specimens of the monthly samples were
used to determine the sex ratio and the dry weight of the
soft tissues. Chi-square analysis was used for sex-ratio
determinations. To determine the dry weight, the body soft
tissues were kept in an oven at 90°C until reaching constant
weight.

Water temperature data during the study period were
supplied by the Marine Station at Mehuin of the Zoolog-
ical Institute, Universidad Austral de Chile.

RESULTS

Mesodesma donacium is a dioecious species as revealed by
microscopic examinations. These results support former
reports of studies on populations of this species occurring
at different locations on the Chilean coast (BROWN &
GUERRA, 1979; TARIFENO, 1980). Monthly analysis of the
proportion of sexes in the mature population of M. do-

nacium revealed a sex ratio of 1:1. Of the total number
examined, 52% of the individuals were males, 46% females,
and 2.1% indeterminate (Figure 1). Sexual dimorphism is
absent.

Male Gonad and Germ Cells

The male gonad consists of numerous follicles located
in the visceral mass surrounding the intestinal coils. The
follicles vary in shape and size and are delimited by a thin,
cellular, enveloping membrane (Ancel’s layer) (Figure 2).
Fibroblast-like cells with spindle-shaped nuclei are seen
in the follicle walls (Figures 3, 4). The cytoplasm of these
cells is difficult to visualize.

In the period of maximum gonadal activity, the follicles
are crowded with cells at different stages of spermatogen-
esis. The cells of particular stages can be recognized by
their nuclear features (shape, size, and staining properties)
and by their location in the gonadal follicles (Figure 5).

Explanation of Figures 2 to 7

Figure 2. Topographical view of the male gonad of Mesodesma
donacium. The well delimited follicles (F) show diversity in size
and shape and occupy the visceral mass (mesosoma) surrounding
the intestine (I). x20.

Figure 3. Primary spermatogonia (spgl) and secondary sper-
matogonia (spg2) lying in the periphery of the follicle. Close to
the spermatogonia, the nucleus of a supporting cell (sc) can be
seen. The spindle-shaped nucleus (arrow) is from a cell of the
follicle wall. x 500.

S. Peredo et al., 1987

Page 57

Figure 4. Primary spermatogonia showing some mitotic figures.
A spindle-shaped nucleus from a cell of the follicle wall (arrow)
is visible and a supporting cell nucleus (sc) is seen next to the
germ cells. x 500.

Figure 5. Germ cells within a male gonadal follicle. Primary
spermatocytes (arrows) are in single-cell columns oriented from
the walls (W) toward the lumen of the follicle (L). x 200.

Figure 6. Primary spermatocytes (spcl) showing meiotic figures
(arrows). Next to the primary spermatocytes, a cluster of sec-
ondary spermatocytes is interspersed with spermatids (spd). The
nuclei of these two cell types are hardly distinguishable. 500.

Figure 7. Clusters of spermatids (spd). Spermatids in more ad-
vanced stages of differentiation (arrow) form radially oriented
columns with the flagella oriented toward the center of the fol-
licles. x 500.

Page 58

The Veliger, Vol. 30, No. 1

Explanation of Figures 8 to 14

Figure 8. Radially oriented columns of spermatozoa and advanced
spermatids. Bundles of flagella occupy the lumen (L) of the
gonadal follicle. x 500.

Figure 9. Dense mass of amoebocytes within a follicle. The
nucleus of a supporting cell (arrow) can be seen. 500.

Figure 10. A gonoduct (G) in the interstitial tissue (IT). x 200.
Figure 11. Topographical view of the female gonad of Mesodesma
donacium. The follicles (F) in the visceral mass surround the
intestine (1). x20.

S. Peredo et al., 1987

Primary spermatogonia: These spermatogonia have large
(about 3 wm diameter) spherical or slightly oval nuclei
with scanty and finely granular chromatin and one or more
conspicuous nucleoli (Figure 3). Primary spermatogonia
are less numerous than secondary spermatogonia and lie
against the membrane enveloping the follicles. Occasion-
ally, mitotic figures can be seen in this type of spermato-
gonia (Figure 4).

Secondary spermatogonia: Spermatogonia of this type
have smaller nuclei (2.0-2.5 um) and stain more heavily
than the nuclei of primary spermatogonia. Secondary sper-
matogonia are more numerous than primary spermato-
gonia and lie close to them (Figure 3).

Primary spermatocytes: These cells form numerous,
compact clusters. They have small nuclei (about 1.8 wm
in diameter) that vary in appearance as the chromatin
assumes different consistencies and locations within the
nucleus. The chromosomes can be scattered in the nucleus
or they may be polarized at the periphery, showing typical
figures of meiotic prophase (Figure 6).

Secondary spermatocytes: Secondary spermatocytes are
seen less commonly than primary spermatocytes. They
occur in groups generally intermingled with spermatids,
thus forming mixed cell groups. The nuclei of secondary
spermatocytes are very similar to those of spermatids (Fig-
ure 6).

Spermatids: These cells have small, round nuclei with
granular and heavily staining chromatin. They form com-
pact clusters with secondary spermatocytes located toward
the center of the follicles (Figure 6). Spermatids in more
advanced stages of differentiation form radially oriented
columns with the flagella oriented toward the center of the
follicles (Figure 7).

Spermatozoa: Spermatozoa are formed in the center of
the follicles where they accumulate. The mature sper-
matozoon has a small round head (1.0 um in diameter).
The chromatin is dense and stains homogeneously. To-
gether with advanced spermatids, mature spermatozoa form
columns oriented toward the center of the follicles with
bundles of flagella occupying the lumina (Figure 8). Owing
to the small size of the sperm head, it is not possible to
visualize with the light microscope such structures as the
acrosome and middle piece described in the sperm of other
bivalves (RETZzIus, 1904, 1905; FRANZEN, 1955, 1969, 1983;
OCKELMANN, 1964; THOMPSON, 1973; POPHAM, 1974).

—
Figure 12. Oogonium (arrow) embedded in the follicle wall. Next

to it a previtellogenic oocyte (po) is seen bulging from the follicle
wall. x 500.

Figure 13. Vitellogenic oocytes of various sizes and shapes pro-
truding into the lumen (L) of the follicle. An oocyte with a slender
stalk (arrow) can be seen. x 200.

Page 59

Somatic cells—Supporting cells: These cells have a pale
and irregularly shaped nucleus with a prominent nucleo-
lus. The cytoplasm is not visible. Supporting cells are seen
next to the follicle walls and intermingled with sperma-
togonia (Figures 3, 4). Cells of this type are seen in the
connective tissue within the follicles when the latter are
empty or partially full of gametes.

Amoebocytes: These cells have a nucleus of a size sim-
ilar to that of the primary spermatocytes, but amoebocyte
nuclei are darkly and homogeneously stained and placed
toward one edge of the cytoplasm. These cells are especially
abundant in follicles that contain residual gametes (Figure
9).

The gonoducts are branched and smaller in diameter
than follicles; the walls are lined with ciliated cells, which
define a narrow lumen. Gonoducts are seen in the inter-
stitial connective tissue that surrounds the gonadal follicles
(Figure 10).

Female Gonad and Germ Cells

As in the male, the female gonad of Mesodesma donacium
is a branched organ embedded in the visceral mass. Nu-
merous follicles surround the intestinal coils. The follicles
are irregular in size and shape, and are delimited by a
connective tissue wall (Figure 11).

In the follicles, germ cells at different stages of devel-
opment can be recognized by their size, shape, and staining
properties.

Oogonia: Oogonia are embedded in the follicle walls, fre-
quently in small groups or “nests.” The nucleus of an
oogonium is spherical, with reticulate and heavily stained
chromatin; a nucleolus is not visible (Figure 12). The
cytoplasm is scanty or not visible.

Previtellogenic oocytes: The shape of previtellogenic oo-
cytes may be square, oval, triangular, or cylindrical. The
scarce cytoplasm is basophilic and bulges from the follicle
walls. The nucleus is large, stains lightly, and has disperse
chromatin that is usually peripherally placed and prom-
inent; there is a basophilic nucleolus (Figure 12).

Vitellogenic oocytes: The size of vitellogenic oocytes var-
ies with the amount of yolk accumulated. As the oocytes
grow they elongate and protrude into the center of the
follicles. The basal region of the cytoplasm is thinner than
the distal end, forming a stalk that attaches oocytes to the
follicle walls. The nucleus is prominent (Figure 13).

Figure 14. Vitelline (full-grown) oocytes in follicles. The am-
phinucleolus (arrow) can be seen in one of them. Amoebocytes
(am) are seen as dense granular bodies, yellowish in sections.
x 200.

Page 60

The Veliger, Vol. 30, No. 1

Explanation of Figures 15 to 20

Figure 15. Section of gonad tissue from a male Mesodesma do-
nacium in the early active stage. Gonadal follicles are small and
well delimited. Germinal cells are beginning to invade the in-
trafollicular spaces.

Figure 16. Section of gonad tissue from a male M. donacium in

the late active stage. Most of the follicles are almost full of
gametes, with small portions of connective tissue remaining. x 20.

Figure 17. Section of gonad tissue from a male M. donacium in
the ripe stage. Mature sperm form dense masses. Follicles are
expanded with their limits poorly delimited. x 20.

Se Reredorchala 9 Si

Mature oocytes (morphologically mature): Vitelline oo-
cytes are larger than early oocytes and are oval or round.
These oocytes have become free of the follicle wall and
have moved into the lumen. The germinal vesicle is intact
with dispersed chromatin and stains lightly. One or more
nucleoli can be seen with eosinophilic and basophilic areas
(amphinucleoli). The cytoplasm is loaded with vitelline
platelets. The size of mature oocytes ranges from 35 to 48
um in diameter, with an average of 41 um (Figure 14).

Somatic cells: Cells similar to the supporting cells of the
male follicles can be seen in the female follicles, close to
the follicle walls. In the interstitial tissue and in follicles
containing residual gametes, one can see amoebocytes hav-
ing the same features described for those of the male gonad.
These cells are frequently seen as dense, yellowish, gran-
ular bodies in the female follicles.

Gonadal Cycle

Histological examination of the gonads in Mesodesma
donacium allows recognition of the following stages of de-
velopment: early active, late active, ripe, partially spawned,
spent, and recovery.

Male gonad —FEarly active stage: This is a phase of in-
tense gamete proliferation and development. Gonadal fol-
licles are rather small and are clearly demarcated by rel-
atively thick walls. The interstitial tissue is abundant and
disseminated among the gonadal follicles. Germinal cells
are beginning to invade the intrafollicular spaces (Figure
15). Primary and secondary spermatogonia are close to the
thickened follicular walls. Primary spermatocytes prolif-
erate toward the lumina. Occasional spermatids at an ini-
tial stage of differentiation can be seen close to primary
spermatocytes toward the center of the follicles. Most of
the intrafollicular spaces are filled with connective tissue
in which supporting cells can be seen. Supporting cells can
also be seen close to the follicular walls.

Late active stage: The remaining spermatogenic stages
are seen in the late active stage. Primary spermatogonia
are now scarce. In contrast, secondary spermatogonia, pri-
mary spermatocytes, and spermatids are numerous. Sper-
matozoa can also be visualized at this stage of gonadal
development. The sperm form radially oriented columns
with the tails toward the center of the follicles. Germinal
cells do not completely fill the follicles; small portions of
the follicles contain connective tissue (Figure 16).

Ripe stage: Gonadal follicles are expanded in the ripe

—

Figure 18. Section of gonad tissue from a male M. donacium in
the partially spawned stage. Follicles still contain sperm but these
are less numerous than in the ripe stage. Spermatids and primary
spermatocytes are located toward the periphery of the follicles.
x 50.

Figure 19. Section of gonad tissue from a male M. donacium in

Page 61

phase with their limits poorly defined. Mature sperm form
dense masses in the follicles of clams in the ripe stage
(Figure 17). Cells in early stages of spermatogenesis are
much less numerous at the periphery of follicles than are
sperm.

Partially spawned stage: Partially spawned follicles
still contain sperm but these are less numerous than in the
ripe stage. Spermatids and primary spermatocytes can be
seen located toward the periphery of the follicles (Figure
18).

Spent stage: Most of the follicles contain no sperma-
tozoa or very few, and the lumina are empty (Figure 19).

Recovery stage: Gonadal follicles at this stage are emp-
ty, except for residual gametes. Close to the follicular walls
lie supporting cells and numerous amoebocytes. The in-
terstitial tissue has increased, branching from the intestine
and surrounding the follicles (Figure 20).

Female gonad—FEarly active stage: In the early active
stage there is an intense proliferation and growth of ga-
metes. Gonadal follicles are small and well delimited by
thickened walls. Interstitial tissue is abundant. Embedded
in the follicular walls are oogonia and, bulging to the center
of the follicles, previtellogenic oocytes can be seen. Vitel-
logenic oocytes of different size and shape lie at the pe-
riphery of the follicle walls and the cytoplasm extends into
the lumen of the follicles (Figure 21).

Late active stage: In the late active phase, vitellogenic
oocytes are more numerous than in the early active stage.
In addition to vitellogenic oocytes of various sizes, some
mature oocytes are free in the lumina of the follicles (Fig-
ice 27).

Ripe stage: Ripe gonads typically have a dense ap-
pearance because the follicles are crowded together and
filled with mature (full-grown) oocytes (Figure 23).

Partially spawned: In partially spawned gonads a few
vitelline (mature) oocytes are free in the lumen of the
follicles and some vitellogenic oocytes are attached to the
walls. Less often, follicles are devoid of ripe oocytes (Figure
24).

Spent stage: In spent gonads most of the follicles are
devoid of ripe gametes, with few residual oocytes. Other
follicles, less numerous, contain a few full-grown and even
vitellogenic oocytes (Figure 25).

Recovery stage: In the recovery stage most of the fol-
licles are completely devoid of gametes, although some
follicles have a few residual oocytes. Amoebocytes are pres-
ent within the follicles, close to the walls and in the center

the spent stage. Almost all of the follicles contain no spermatozoa,
but a few others still have scarce gametes. x 20.

Figure 20. Section of gonad tissue from a male M. donacium in
the recovery stage. Follicles are empty except for residual ga-
metes. Interstitial tissue has increased, branching from the in-
testine and surrounding the follicles. x 20.

Page 62

y 71cm
KD of Gry

Ge

2.6006",

: ba BD

The Veliger, Vol. 30, No. 1

;
a ,
-

ae a | <4 hy’ ick 56 e
| Ewe ol
Mee ee N ‘ o As . 4 od 26

Explanation of Figures 21 to 26

Figure 21. Section of gonad tissue from a female Mesodesma
donacium in the early active stage. Embedded in the follicular
walls are oogonia, and vitellogenic oocytes can be seen bulging
toward the center of the follicles. x 50.

Figure 22. Section of gonadal tissue from a female M. donacium

in the late active stage. Vitellogenic oocytes are larger and more
numerous than in the former stage of gonad development. Some
vitelline oocytes can be seen free in the lumina of the follicles.
x50.

Figure 23. Section of gonad tissue from a female M. donacium

Sa BReredoreeal 198i,

Page 63

Table 1

Percentage frequency of the sampled population of Mesodesma donacium from Queule Beach in each reproductive phase
during the study period.

Early active Late active Ripe Partly spawned Spent
Males Females Males Females Males Females Males Females Males Females
Date No. % No. % No. % No. % No. % No. % No. % No. % No. % No. %
Sept. 83 0 0 0 0 8 53 12 87 qo ef 4 13 Q @ 0) 0) 0 O 0 O
Oct. 83 0 (0) 0 0 1 8 7 70 12 92 3 30 0 O 0 0) 0 O 0 Oo
Nov. 83 0 0) 0 0) 0) 0) 3 1) 15 100 13 81 0 0) 0 0) 0) 0 0) 0)
Dec. 83 0) 0 0 0) 0) © OO 3 24 0 O 10 76 11 100 0 O ORO
Jan. 84 0 0 0) 0) 0). © 0 © 1 7 0 O 14 93 15 100 0 O 0 O
Feb. 84 0 0 0 0 © © @ ©@ 2 13 QO 2B ‘AB 11 100 ii 73 0 O
Mar. 84 0 0 0 0 0 O 0). 0 (0) O20 6 43 5 33 3 SY 10 66
Apr. 84 0 0 0) 0) 0 0 @ @ 0) 0 0 O 2D M2 3 25 14 88 5
May 84 —_- —
Jun. 84 16 100 23 100 OQ © © © 0) 0) 0 O 0 O 0) 0) 0 O 0 O
Jul. 84 9 50 18 100 9 50 Q @ 0 0 OPO Ono 0 0) 0 O Q @
Aug. 84 0 0 13. 86.6 14 80 DB Mx! 3 20 0 O 0 O 0 0 @ © 0 O

of the follicles. Interstitial tissue occurs in the spaces be-
tween the loosely arranged follicles (Figure 26).

Annual Reproductive Cycle

Histological examination of the gonadal sections re-
vealed a seasonality of gonadal stages (Table 1, Figures
27, 28). During the study period (August 1983-November
1984) male clams in the late active stage were encountered
from July to September and females from August through
September. In September 1983, 53% of the males and 87%
of the females were in this stage. During October, 92% of
the males and 30% of the females were in the ripe stage.
Ripe males (100%) and females (81%) were most abundant
in November.

Clams in a spawning condition were first encountered
in December and were last observed in the early April
1984 samples. Males in this stage were most abundant in
January (93%) and then declined in the following months
(February, March, and April) to 13%, 43%, and 12%
respectively. Females in partially spawned stage were most
abundant (100%) from December through February and

—

in the ripe stage. The gonad has a dense appearance with follicles
crowded together and filled with vitelline (full-grown) oocytes.
x 50.

Figure 24. Section of gonad tissue from a female M. donacium
in the partially spawned stage. Some follicles have a few vitelline
and vitellogenic oocytes attached to the walls. Other, less nu-
merous follicles are completely devoid of oocytes. x 50.

Figure 25. Section of gonad tissue from a female M. donacium
in the spent condition. In this stage, most of the follicles are

then dropped to 33% and 25% in March and April re-
spectively.

Spent clams were present from February to April, with
the highest percentage of males (73%) occurring in Feb-
ruary and the highest percentage of spent females (75%)
in April. Histological examination of gonads during April
revealed that clams in the spent stage had already initiated
the resting or recovery stage.

Even though no samples were collected in May 1984,
the observed histological features of the gonads in April
and in June 1984 suggested that during May, clams were
in the recovery stage, a condition observed in part of the
population in April.

In June, 100% of the males and females were in the
early active stage. During July, 50% of the males were in
the early active phase and the other 50% were the first
individuals encountered in the late active stage. In the same
month (July), 100% of the females were still in the early
active phase.

In August 1984, the last month in which samples were
histologically examined, 80% of the males and 10% of the
females were in the late active stage. This low percentage

devoid of gametes, with a few residual oocytes. Other, less nu-
merous follicles contain some full grown and even vitellogenic
oocytes. 50.

Figure 26. Section of gonad tissue from a female M. donacium
in the recovery stage. Most of the follicles are completely devoid
of gametes, but other, less numerous follicles contain residual
gametes. Interstitial tissue extends from the intestine wall among
the loosely arranged follicles.

Page 64

iheWeligery Volks OMNossl

early active

late active

ripe

partially spawned

spent

recovery

eoevoe2en00e2e2e820820820288 888888888 FSCS 8 Ce
ool MBM Leal bi
A %%

Figure 27

Reproductive cycle of Mesodesma donacium from Queule Beach during the study period. The length of each shaded
area represents the percentage frequency of the population in each reproductive phase.

shows that August corresponds to the beginning of the late
active phase in females. This stage extends through Sep-
tember and October as revealed by the histological ex-
amination of gonad sections at the beginning of the study
period.

The dry weight of specimens changed throughout the
year. A first increase in the dry weight was shown in
November-December and then it decreased in January.
A second increase in the dry weight of specimens was
observed in March, followed by a progressive decrease
from that month until the end of the study (Figure 29).

DISCUSSION

Male germ cells recognized in Mesodesma donacium cor-
respond to the usual types observed in the spermatogenesis
of various marine bivalves (SASTRY, 1977), thus indicating
that this process in M. donacium follows the same general
plan described elsewhere in invertebrates as well as in
vertebrates (ROOSEN-RUNGE, 1977).

Two types of spermatogonia can be recognized (Figure
3). Primary spermatogonia derived from primordial germ
cells proliferate and give rise to secondary spermatogonia,
which are definitive spermatogonia as these are the end
products of spermatogonial mitosis (Figure 4). Secondary
spermatogonia directly give rise to primary spermatocytes.

Secondary spermatocytes were difficult to identify. Ap-
parently meiotic division is rapid at this stage; consequent-
ly, secondary spermatocytes would be very transient cells,

giving rise to spermatids (GIESE & PEARSE, 1977;
ROOSEN-RUNGE, 1977). Probably the nuclei of secondary
spermatocytes are very similar to those of initial spermatids
and thus they cannot be distinguished using light micros-
copy.

Neither cells of atypical spermatogenesis nor atypical
sperm, described in several marine bivalves and gastropods
(LOOSANOFF, 1937a, 1953; COE & TURNER, 1938; ANKEL,
1958; BULNHEIM, 1962; NISHIWAKI, 1964; OCKELMANN,
1965; SHAW, 1965), were observed in the spermatogenesis
of Mesodesma donacium, thus indicating that in this species
atypical spermatogenesis does not occur or occurs very
rarely.

Somatic cells observed within gonadal follicles in Me-
sodesma donacium correspond to two different functional
types of cells. The first and more abundant type corre-
sponds to supporting and, possibly, nutritional cells. So-
matic cells of the second type are phagocytic cells (amoe-
bocytes) which are similar to those called cell Type C by
TRANTER (1958). Phagocytic cells have been described in
the gametogenesis of several bivalves. Such cells also have
been assigned a nutritional role (LOOSANOFF, 1937b;
TRANTER, 1958; WILSON & HODGKIN, 1967).

Oogenesis in Mesodesma donacium has the usual char-
acteristics described for other marine bivalves. It was not
possible to distinguish primary and secondary oogonia, as
described in other mollusks (TRANTER, 1958; RAVEN, 1961).
Diffuse chromatin of the nucleus of previtellogenic oocytes
indicates that these oocytes are in the vegetative phase

S. Peredo ef al., 1987

ie GAMETOGENESIS
SPAWNING

11

1983

Page 65

GAME TOGENESIS

RECOVERY,

1984

Figure 28

Monthly mean, and standard deviation, of water surface temperature at Mehuin (39°25’S, 73°13’W), located next
to Queule Beach, during the study period. Corresponding periods of gametogenesis, spawning, and recovery are

indicated for reference.

(RAVEN, 1966), that is, in meiosis arrested at early pro-
phase.

Growing oocytes with a cytoplasmic stalk have also been
described in several marine bivalves (SALEUDDIN, 1964;
Ropes, 1968; PoRTER, 1974; DE VILLIERS, 1975; RAE,
1978) including Chilean bivalves (CIFUENTES, 1975;
LOZADA & REYES, 1981; LOZADA & BusTos, 1984) and
also in freshwater bivalves (BEAMS & SEKHON, 1966;
ZUMOFF, 1973; PEREDO & PARADA, 1984). BEAMS &
SEKHON (1966) assign a mechanical and also a possible
nutritional role to the cytoplasmic stalk. Mature (full-
grown) oocytes show the germinal vesicle intact, thus in-
dicating that meiosis is not completed within the gonadal
follicles, a situation also described in other bivalves such
as Crassostrea virginica (GALSTOFF, 1937), Spisula solidis-
sima (ROPES, 1968) and Donax serra (DE VILLIERS, 1975).
This situation is turn differs from that in other bivalves
such as Cyprina islandica and Venus mercenaria (LOOSANOFF,
1953), V. striatula (ANSELL, 1961), Mya arenaria and Mer-
cenaria mercenaria (STICKNEY, 1963), in which at the time
of ovulation, the oocytes possess broken down germinal
vesicles and the chromosomal spindle is formed. Possibly
Mesodesma donacium oocytes, like S. solidissima, requires
fertilization for germinal vesicle breakdown to occur and,

consequently, meiosis to be re-initiated (ALLEN, 1953;
‘TUMBOH-OERI & KOIDE, 1982). Therefore, in Mesodesma
donacium, full-grown oocytes contained in gonadal follicles
reach only morphological maturity; physiological maturity
is achieved once they have left the gonad.

Reproductive Cycle

Histological examination of gonad sections during the
study period allowed us to determine that the reproductive
cycle of Mesodesma donacium is a biological event with
annual periodicity. A maturation period occurs from June
through November (winter and spring) and a spawning
period extends from December to April (summer-early
autumn), followed by a short recovery period during May,
and then the start of a new cycle.

The percentage of individuals of the population in dif-
ferent stages of gonadal development during the study pe-
riod (Table 1) indicates that males and females are in
synchrony at the beginning of the maturation period (early
active stage) because practically 100% of the males and
females are in the early active stage during June. This
synchrony disappears as the maturation period proceeds
(late active and ripe stages), such that during October, 92%

Page 66
DW.
(g)
50
*.
45 oes .

B54 een ee
WY

30 :

25

1983

The Veliger, Vol. 30, No. 1

1984

Figure 29

Seasonal changes in soft tissues in Mesodesma donacium from Queule Beach, calculated for a standard animal of

70-mm shell length (males —:— and females ---*-—-).

of the males are in the late active stage, whereas in that
month only 30% of the females are in the same stage of
gonadal development. In November, 100% of the males
and 81% of the females have reached the ripe stage. The
differences in the timing of the gonadal condition of the
two sexes is attributable to the different rate at which
spermatogenesis and oogenesis proceed, the latter being a
slower process mainly owing to the accumulation of food
reserves in the oocytes.

The spawning period starts in December in both sexes,
as no specimens in that condition were registered before
then. Spawning Is partial and asynchronous. In December,
100% of the females were in the partial spawning stage.
In males, the highest proportion of individuals in that
condition was observed one month later (January). Even
though in males the onset of spawning occurs gradually,
this stage ends more abruptly than in females: by April,
88% of the males were in the spent stage whereas only
75% of the females were in that stage in the same month.

Although adverse climatic conditions hampered sam-
pling in May, the histological characteristics of gonads in
both sexes in the month immediately before (April, 1984)
and immediately after (June, 1984) indicate that during
May, gonads are in the recovery phase, a stage already
present in a proportion of the individuals examined in
April. This indicates an overlap between the spent and
recovery stages, the majority of the population being found
in the latter stage during May.

Although the percentages of clams in different stages of

gonadal development show that the entire population of
Mesodesma donacium does not reach ripeness at the same
time, the majority of the population was ripe at the be-
ginning of the spawning phase. This shows that the breed-
ing period of M. donacium in the study area is limited to
a certain period of the year (summer-early autumn) coin-
cident in this respect with several bivalves that have an
annual reproductive cycle with only one spawning period.
A similar situation has been described in Mercenaria mer-
cenaria and Cyprina islandica (LOOSANOFF, 1937b, 1953),
Mya arenaria (COE & TURNER, 1938; ROPES & STICKNEY,
1965; PORTER, 1974), Venus striatula (ANSELL, 1961) and
Macoma balthica (LAMMENS, 1967) among others. The
congeneric species Mesodesma mactroides that inhabits the
Atlantic coast of South America has two breeding periods:
October-December and February-March (OLIVIER et al.,
1971).

The results of the present study differ from those re-
ported on the reproductive cycle of populations of Meso-
desma donacium occurring at other latitudes on the Chilean
coastline. BROWN & GUERRA (1979) reported that the M.
donacium population in Guanaqueros, northern Chile
(30°15’S, 71°40’W) spawns in spring-summer, with the
maximal intensity at the beginning of November, followed
by a resting period. TARIFENO (1980) determined the mat-
uration period of M. donacium at Laguna Beach in the
Valparaiso area, central Chile (32°30’'S, 71°30'W) to be
during the fall-winter season (April through July). There,
the maximal population ripeness was reached in mid-win-

S. Peredo et al., 1987

ter and the spawning season extended from the end of the
winter to the beginning of spring. The resting period of
that population extended from spring to mid-autumn (Oc-
tober through May).

The observed differences in the timing of the different
phases of the reproductive cycle in Mesodesma donacium
in the different latitudes are probably ascribable to local
variations of environmental factors, the major ones being
water temperature and the availability of food. Several
authors have reviewed the influence of temperature on the
reproductive cycle of marine invertebrates. As an external
factor, temperature can exert a selective pressure in the
determination of the breeding season of a species (ultimate
factor) and its fluctuations act as external clues that syn-
chronize the reproductive cycle of a species (proximate
factor) (GIESE, 1959; FRETTER & GRAHAM, 1964; GIESE
& PEARSE, 1977).

TARIFENO (1980) suggests that the increase in water
temperature variation that occurs at the end of the winter
could trigger spawning of surf clams at Valparaiso. In the
area of the present study, the greatest monthly thermal
changes occurred in November 1983 and 1984, with the
difference between the monthly maximum and minimum
temperature being 1.3°C and 1.1°C respectively. Although
the maximal thermal oscillations coincided with the end
of the maturation period and the beginning of the spawning
season, this factor alone, with its meager change, probably
does not trigger spawning of the Mesodesma donacium pop-
ulation at Queule Beach. The spawning season observed
in the present study also coincides with the period of in-
creasing surface water temperature in the area (Figure
28). Therefore, perhaps spawning of the surf clam pop-
ulation at Queule Beach is due to the combined effect of
both variables of water temperature: the increase of water
temperature and the increase in the monthly thermal os-
cillation that occurs from November on.

The increase in the phytoplankton biomass registered
in the area from spring to mid-autumn (Toro, 1984)
represents a greater food supply for planktotrophic organ-
isms. In this way, the reproductive cycle of Mesodesma
donacium is timed such that gamete emission, from De-
cember on, allows larvae to hatch during the season of the
greatest abundance of phytoplankton in the area, a period
that lasts from November to May (Toro, 1984).

Seasonal changes in the dry weight of specimens (Figure
29) show that the first increase reaches its maximum at
the end of spring (November-December) and then dry
weight decreases in January. This change is due to the
increase in gonad weight at the end of the maturation
period, which is followed by the spawning period. The
second increase in the dry weight of specimens reaches its
maximum in March, after which a progressive decline in
dry weight is observed. These variations may be caused
by the accumulation of food reserves during the period of
food abundance (weight increase) and then by the depletion
of these reserves in the maturation period during the win-
ter—spring seasons.

Page 67

From the above discussion it can be concluded that Me-
sodesma donacium has evolved a reproductive strategy in
which gametes are produced during the winter-spring pe-
riod, utilizing food reserves stored in the gonad itself or in
other body tissues. Furthermore, this strategy increases
larval survival through gamete emission during the sum-
mer and beginning of fall so that clam larvae find an
adequate food supply at the time of hatching.

ACKNOWLEDGMENTS

This work was supported with funds from the Comision
de Investigacion Catholic University of Chile-Temuco. The
authors are indebted to the Zoological Institute, Univer-
sidad Austral de Chile for furnishing the unpublished water
temperature records for 1983-84 from the Biological Ma-
rine Station in Mehuin. The authors thank Katherine
Bragg for reading the manuscript.

LITERATURE CITED

ALLEN, R. D. 1953. Fertilization and artificial activation in
the egg of the clam, Spisula solidissima. Biol. Bull. 105:213-
239.

ANKEL, W. E. 1958. Beobachtungen und uberlunger zur Mor-
phogenese des atypischen Spermiens von Scala clathrus L.
Zool. Anz. 160(11-12):261-276.

ANSELL, A. D. 1961. Reproduction, growth and mortality of
Venus striatula (Da Costa) in Kames Bay, Millport. Jour.
Mar. Biol. Assoc. U.K. 41:191-215.

BeaMs, H. W. & S. S. SEKHON. 1966. Electron microscope
studies on the oocyte of the fresh-water mussel (Anodonta)
with special reference to the stalk and mechanism of yolk
deposition. Jour. Morph. 119:477-501.

Brown, D. & R. GUERRA. 1979. Estados en el ciclo estacional
de la gonada de la macha Mesodesma donacium (Lamark,
1818) en la bahia de Guanaqueros. Arch. Biol. Med. Exp.
12(4):500.

BULNHEIM, H. P. 1962. Untersuchumgen zum spermatozoen
Dimorphismus von Opalia crenimarginata (Gastropoda Pro-
sobranchuia). Z. Zellforsch. Microsk. Anat. 56:300-343.

CIFUENTES, A. S. 1975. Estudio sobre la biologia y cultivo de
Mytilus chilensis Hupe, 1854 en Caleta Leandro. Tesis U.
de Concepcion-Chile. 124 pp.

Coe, W.R. & H. J. TURNER. 1938. Development of the gonads
and gametes in the soft-shell clam (Mya arenaria). Jour.
Morph. 62:91-111.

DE VILLIERS, G. 1975. Reproduction of the white sand mussel
Donax serra Roding. Sea Fisheries Branch Investigational
Rept., South Africa No. 102: 33 pp.

FRANZEN, A. 1955. Comparative morphological investigations
into the spermiogenesis among Mollusca. Zool. Bidr. Upp-
sala 30:399-456.

FRANZEN, A. 1969. Comparative spermatology. /n: Baccio Bac-
ceti (ed.), Proc. 1st Inst. Symp. (Rome Siena) Accademia
Nazionale Dei Lincei. No. 137:1-46.

FRANZEN, A. 1983. Ultrastructural studies of spermatozoa in
three bivalves species with notes on evolution of elongated
sperm nucleus in primitive spermatozoa. Gam. Res. 7:199-
214.

FRETTER, V. & A. GRAHAM. 1964. Reproduction. Pp. 127-
163. In: K. M. Wilbur & C. M. Yonge (eds.), Physiology of
Mollusca. Academic Press: New York.

Page 68

GatstorF, P.S. 1937. Spawning and fertilization of the oyster
Ostrea virginica. Pp. 537-539. In: Galstoff et al. (eds.), Cul-
ture methods for invertebrate animals. Comstock: Ithaca,
New York.

GigsE, A. C. 1959. Comparative physiology: annual repro-
ductive cycles of marine invertebrates. Ann. Rev. Physiol.
21:547-576.

GigsE, A. C. & J. S. PEARSE. 1977. General principles. Pp. 1-
49. In: A. C. Giese & J. S. Pearse (eds.), Reproduction of
marine invertebrates. Academic Press: New York.

LAMMENS, J. J. 1967. Growth and reproduction in a flat pop-
ulation of Macoma balthica (L.). Neth. Jour. Sea Reb. 3:315-
382.

LoosanorF, V. L. 1937a. Development of the primary gonad
and sexual phases in Venus mercenaria Linnaeus. Biol. Bull.
72:387-405.

LoosanorrFr, V. L. 1937b. Seasonal gonadal changes in adult
clams, Venus mercenaria (L.). Biol. Bull. 72:406-416.
LoosanorF, V. L. 1953. Reproductive cycle in Cyprina islan-

dica. Biol. Bull. 104:146-155.

Lozapa, E. 1968. Contribucion al estudio de la cholga Aula-
comya ater en Putemun (Mollusca, Bivalvia, Mytilidae). Biol.
Pesq. Chile 3:3-39.

Lozapa, E. & H. Bustos. 1984. Madurez sexual y fecundidad
de Venus antiqua King y Broderip 1835 en la Bahia de Ancud
(Mollusca: Bivalvia: Veneridae). Rev. Biol. Mar. Valpa-
raiso. 20(2):91-112.

Lozapa, E. & P. Reyes. 1981. Reproductive biology of a
population of Perumytilus purpuratus at El Tabo, Chile. Ve-
liger 24:147-154.

Lozapa, E., J. ROLLERI & R. YANEZ. 1971. Consideraciones
biologicas de Choromytilus chorus en dos sustratos diferentes.
Biol. Pesq. Chile 5:61-108.

NIsHIWAKI, S. 1964. Phylogenetical study on the type of the
dimorphic spermatozoa in Prosobranchia. Sci. Rept. Tokyo
Kyoiku Daigaku (B) 11:237-275.

OCKELMANN, K. W. 1964. Turtonia minuta (Fabricius), a neo-
taneous veneranacean bivalve. Ophelia 1:121-146.

OCKELMANN, K. W. 1965. Redescription, distribution, biology
and dimorphous sperm of Montacuta tenella Loven (Mol-
lusca, Leptonacea). Ophelia 2:211-222.

OLIVIER, S. R., D. A. CAPEZZANI, J. I. CARRETO, H. E. CuRIs-
TIANSEN, V. J. MORENO, J. E. AISPUN DE MORENO & P.
E. PENCHAZZADEH. 1971. Estructura de la comunidad,
dinamica de la problecién y biologia de la almeja amarilla
(Mesodesma mactroides Desh 1854) en Mar Azul. Proyecto
de Desarrollo Pesquero. Mar del Plata. Argentina. Publ.
No. 27:90 pp.

PEREDO, S. & E. PARADA. 1984. Gonadal organization and
gametogenesis in the fresh-water mussel Diplodon chilensis
chilensis (Mollusca: Bivalvia). Veliger 27(2):126-133.

PEREZ-OLEA, M. 1981. Biologia reproductiva del choro zapato
Choromytilus chorus (Molina 1872) en un estuario del sur de
Chile (Queule, IX Region). Tesis Universidad Austral de
Chile. 35 pp.

PoPpHaM, J. D. 1974. Comparative morphometrics of the ac-
rosome of the sperm of externally and internally fertilizing
sperms of the shipworms (Teredinidae, Bivalvia, Mollusca).
Cell Tiss. Res. 150:291-297.

PorTER, R.G. 1974. Reproductive cycle of the soft-shell clam,

The Veliger, Vol. 30, No. 1

Mya arenaria at Skagit Bay, Washington. Fish. Bull. 72:
648-656.

RakE, J. G. 1978. Reproduction in two sympatric species of
Macoma (Bivalvia). Biol. Bull. 155:207-219.

RAVEN, C. P. 1961. Oogenesis: the storage of developmental
information. Pergamon Press: New York.

RAvEN, C. P. 1966. Morphogenesis: the analysis of molluscan
development. 2nd ed. Pergamon Press: New York.

Retzius, G. 1904. Zur Kenntnis der Spermien der Everte-
braten. Biol. Unters. 9:1-32.

Rerzius, G. 1905. Zur Kenntnis der Spermien der Everte-
braten II. Biol. Unters. 12:79-102.

ROOSEN-RUNGE, E. C. 1977. The process of spermatogenesis
in animals. Cambridge University Press: London.

Ropes, J. W. 1968. Reproductive cycle of the surf clam Spisula
solidissima in offshore New Jersey. Biol. Bull. 135(2):349-
365.

Ropes, J. W. & A. P. STICKNEY. 1965. Reproductive cycle of
Mya arenaria in New England. Biol. Bull. 128:315-327.
SALEUDDIN, A.S.M. 1964. The gonads and reproductive cycle
of Astarte sulcata (Da Costa) and sexuality in A. elliptica

(Brown). Proc. Malacol. Soc. Lond. 36:141-148.

Sastry, A. N. 1977. Reproduction of pelecypods and lesser
classes. In: A. C. Giese & J. S. Pearse (eds.), Reproduction
of marine invertebrates. Academic Press: New York.

SHAW, W. N. 1965. Seasonal gonadal cycle of the male soft
shell clam Mya arenaria in Maryland. U.S. Fish. Wildl. Serv.
Spec. Sci. Rept. Fish. 508:5.

Souis, I. 1967. Observaciones biologicas en ostras (Ostrea chi-
lensis) Philippi de Pullinque. Biol. Pasq. Chile 2:51-82.
Souis, I. & E. Lozapa. 1971. Algunos aspectos biologicos de
la cholga de Magallanes Aulacomya ater Mol. Biol. Pesq.

Chile 5:105-144.

STICKNEY, A. P. 1963. Histology of the reproductive system of
the soft shell clam (Mya-arenaria). Biol. Bull. 125:344-351.

TARIFENO, E. 1980. Studies on the biology of the surf-clam
Mesodesma donacium (Lamarck 1818) (Bivalvia: Mesodes-
matidae) from Chilean sandy beaches. Doctoral Thesis, Uni-
versity of California, Los Angeles. 229 pp.

THompson, T. E. 1973. Euthineuran and other molluscan
spermatozoa. Malacologia 14:167-206.

Toro, J. E. 1984. Determinacion de las fluctuaciones men-
suales de la abundancia y de la biomasa fitoplanctonica en
el estuario del Rio Queule (Chile, IX Region). Rev. Biol.
Mar. Valparaiso 20(1):23-37.

TRANTER, D. T. 1958. Reproduction in Australian pear oysters
(Lamellibranchia) II. Pinctada albina (Lamarck): gameto-
genesis. Austral. Jour. Mar. Freshwater Res. 9:144-158.

TUMBOH-OkrRI, A. G. & S. S. KomDE. 1982. Mechanism of
sperm-oocyte interaction during fertilization in the surf clam
Spisula solidissima. Biol. Bull. 162:124-134.

WALNE, P. 1963. Breeding of the Chilean oyster (Ostrea chi-
lensis Phil.) in the laboratory. Nature 197(4868):676.
WILSON, B. R. & E. P. HODGKIN. 1967. A comparative account
of the reproductive cycle of five species of marine mussels
(Bivalvia: Mytilidae) in the vicinity of Fremantle, Western
Australia. Austral. Jour. Mar. Freshwater Res. 18:175-203.

ZumorrF, C. H. 1973. The reproductive cycle of Sphaerrum
semile. Biol. Bull. 144:212-228.

The Veliger 30(1):69-75 (July 1, 1987)

THE VELIGER
© CMS, Inc., 1987

Oxygen Uptake and the Effect of Feeding in Nautilus

by

M. J. WELLS

Department of Zoology, University of Cambridge, Cambridge, U.K. CB2 3EJ,
Lizard Island Research Station, Queensland, Australia

Abstract.

Specimens of Nautilus pompilius (Linnaeus, 1758) and N. stenomphalus (Sowerby, 1849)

were caught off the Great Barrier Reef. The animals can regulate their oxygen uptake successfully
down to ambient PO.s of 60 mm Hg and beyond at 10-20°C; some individuals reduced the PO, in their
respirometer to 15 mm Hg and lower before ventilation ceased; spontaneous recovery occurred when a
well-oxygenated circulation was restored. The effect of feeding was investigated. There was no sign of
a transient rise and fall in oxygen uptake following a meal, but some indication that, in the longer term,
regular feeding or starvation could double or halve the metabolic rate. Oxygen uptake is very dependent
on temperature, which would make the nightly vertical migrations into shallower, warmer water of
considerable importance in terms of the animal’s energy budget. A crude estimate of this budget suggests
that a 500-g (flesh weight) Nautilus could maintain its normal activity pattern in the sea on about 2 g
(wet weight) of fish per day; a good cropful would last it a month, or considerably longer, as metabolic

rate falls in starvation.

INTRODUCTION

Nautilus is the sole living representative of the many shelled
cephalopod mollusks found in the fossil record. Morpho-
logically, the shells of the four surviving species (N. be-
lauensis Saunders, 1981; N. macromphalus Sowerby, 1849;
N. pompilius Linnaeus, 1758; N. scrobiculatus Lightfoot,
1786; SAUNDERS, 1981) differ rather little from those of
their Palaeozoic ancestors. There is every reason for study-
ing the physiology and behavior of the modern animal; it
is the only model for the extinct species that we have, and
it is arguably more likely to resemble them in its habits
and ecology than are the coleoids.

In 1985, Nautilus pompilius was trapped off the Great
Barrier Reef near Lizard Island, Queensland, as part of
a research program examining the distribution of Nautilus
species (see SAUNDERS, 1981). As well as N. pompilius,
specimens of N. stenomphalus, which may or may not be
a valid species, were found. This was the first time that
N. stenomphalus had been seen alive. As well as the known
N. stenomphalus shell characteristics (open umbilicus and
reduced shell pigmentation compared with N. pompilius,
which it otherwise closely resembles), the animal has a
distinct papillose hood. The data obtained gave no grounds
for separating these two, but the availability of freshly
caught Nautilus at a laboratory with some refrigeration
facilities made possible the collection of fresh data on the
capacity to regulate O, uptake and to survive acute hy-

poxia, as well as information on metabolic rate and feeding,
which is presented here.

MATERIALS anp METHODS

Nautilus specimens were collected off Carter reef, 22 km
(14 miles) NE of Lizard Island. Traps baited with dead
fish and crabs were set on the fore-reef slope in 200 to 400
m from RVS Sunbird of the Lizard Island Research Sta-
tion.

Animals for experiments were brought back to the lab-
oratory ina refrigerated holding tank aboard RVS Sunbird.
At the research station they were housed in a 220-L stock
tank, aerated, and refrigerated; the flow of water through
the stock tank (~250 mL/min) was used to adjust the
temperature. Two 11-L respirometers were enclosed, and
a refrigeration compartment built from polystyrene sheets
around these and the holding tank, from which the res-
pirometers were filled as required. Each respirometer had
a floating lid of polystyrene, so that samples of the water
could be run off through a compartment containing the
electrode from an EIL 7130 oxygen analyzer and returned
to the respirometer. Samples flowing past the oxygen probe
were stirred magnetically. The electrode and collecting
vessel (a beaker with a floating polystyrene lid) were en-
closed in the same refrigerated space as the three aquaria.

Specific oxygen uptake figures are given in terms of flesh
weight, measured when the animals were killed at the end

40

20

LZ19
3909
jaaies Ive ive
14c
1 2 3 4 5)
Hours
18¢
. 18¢
Crue ZS
é 126g
19c
. L226 425g
20c
1 2 3 4 5

Hours

M. J. Wells, 1987

Page 71

(C)
160

140

120

PO, 100
mm Hg

80

60

40

20

LZ29
385g 19¢

LZ29
19¢

390g 17c

}
|
|
|
|
|
l
|
LZ19
|
|
|
|
|
|
I

Hours
Figure 1

Regulation of oxygen uptake by Nautilus in closed respirometers. (a) five runs by a N. pompilius, LZ19 565 g, body
wt. 390 g. (b) two runs by a juvenile N. pompilius/stenomphalus “hybrid,” LZ28, 200 g, body wt. 126 g. And two
by N. pompilius, LZ26, 655 g, body wt. 425 g. (c) two runs to very low oxygen levels by LZ19 and LZ29, another
N. pompilius/stenomphalus “hybrid,” 630 g, body wt. 385 g; in this plot, oxygen uptake is shown for a period

immediately following transfer to well-aerated seawater.

characteristics of the two supposed species.

of the experiments. The oxygen content of the seawater at
100% saturation was taken from data given in CARPENTER
(1966), assuming a chlorinity of 19.05, appropriate for
Lizard Island in December.

The six animals used all remained in good condition
throughout the period in the laboratory. Results from a
seventh, which refused to feed at once when food was
offered, were discarded.

RESULTS
Regulation of Oxygen Uptake

Because of the limitations imposed by refrigeration ca-
pacity, through-flow respirometry was impossible and oxy-
gen uptake had to be measured from the reduction in PO,
in a respirometer. It was therefore important to establish
whether Nautilus can maintain its oxygen uptake in a
declining ambient PO,. Reports on its capacity to regulate

“Hybrids” are specimens showing a mixture of the

in this manner have differed. REDMOND et al. (1978) showed
that it could not do so at 25°C, whereas WELLS & WELLS
(1985) found that the animals regulated successfully down
at least to a PO, of 75 mm Hg in water at 17°C. Figure
1 summarizes a number of experiments made in which
Nautilus progressively reduced the oxygen in their tanks
down to PO,s of 60 mm Hg and beyond (exceptionally to
less than 20 mm Hg) without apparently changing their
rates of uptake, at least until levels of 30 mm Hg and
below were reached. Thus, there is no doubt that this
animal can regulate over a wide range at the temperatures
it normally meets in the sea.

Activity and Q,,,

Oxygen uptake rises by a factor of two or three times
when Nautilus is jetting rather than sitting quietly at 18-
20°C.

Page 72

Table 1

Nautilus. Activity, animal size, and oxygen uptake in mL-
kg-'-min“', along with temperature during run and num-
ber of days since last feeding; representative values from
runs lasting for 1 h or more and ending with PO,s above

60 mm Hg.
No. days
since last
feeding
LZ19. N. pompilius. Mature male
(565 g, body wt. 390 g).
Active, while feeding 1.006 (19°C)
Quiet 0.532 (19°C) 0
Quiet 0.207 (12°C) 4
LZ24. N. stenomphalus. Mature female
(480 g, body wt. 310 g).
Feeding 1.151 (21°C)
Quiet 0.390 (18.5°C) 4
Quiet 0.189 (13°C) 5

LZ206. N. pompilius. Mature male
(655 g, body wt. 425 g).
Active 1.072 (20°C) 1
Quiet, following activity 0.814 (19°C) 1
LZ28. N. pompilius/stenomphalus “hybrid.”
Immature male (200 g, body wt. 126 g).
Active 1.516 (18°C) 2
Quiet 0.499 (17.5°C) 4
LZ29. N. pompilius/stenomphalus “hybrid.”
Mature male (630 g, body wt. 385 g).
After extreme hypoxia
(see Figure 1c) 0.852 (19°C)
Quiet 0.268 (17.5°C) 6
LZ30. N. pompilius/stenomphalus “hybrid.”
Mature male (810 g, body wt. 607 g).
Active 0.605 (18°C) 4
Quiet 0.256 (17°C) 3

“Hybrids” were individuals showing a mixture of the char-
acteristics of the two supposed species.

Figure 2 shows specific oxygen consumption plotted
against temperatures for all runs lasting longer than 30
min made with mature animals at rest (or at least not
noted as “active”; they were not kept under continuous
observation). Oxygen uptake rises with increasing tem-
perature, a matter that could be important to an animal
that makes daily vertical migrations on reef slopes (WARD
et al., 1984). The Q,, computable from this data is 4.3,
but the scatter is large and little reliance should be placed
on the accuracy of this figure.

Numbers alongside the outlying values in Figure 2 show
the number of days since the individual concerned was last
fed. Feeding increases the metabolic rate, fasting reduces
it.

The Veliger, Vol. 30, No. 1

The Capacity to Survive Periods of Acute Hypoxia

Nautilus can withdraw into its shell, blocking the en-
trance with the hood. As it cannot then ventilate, one would
expect the animal to be resistant to intermittent hypoxia.
In the present series of experiments animals were allowed
to deplete the oxygen in their respirometers down to PO,s
of 20 mm Hg and lower, on six occasions. In the two most
extreme cases, ventilation eventually ceased. The tentacles
of these animals were extended, flaccid, and the animals
were, to all external appearances, dead. They nevertheless
reacted at once when touched, drawing back into the shell
and (or) beginning to ventilate afresh. Vigorous ventilation
began when the seawater in the respirometer was aerated.
In the single instance when oxygen uptake was measured
immediately after the restoration of oxygen-rich seawater
(see Figure 1), this was greatly enhanced, suggesting re-
payment of an oxygen debt. No attempt was made to
quantify this.

Effects of Feeding on Oxygen Uptake

Figure 3 summarizes the effect of feeding one animal
five times in the course of nine days, four of the meals
being on successive days. On three of the five occasions
there was a marked rise in oxygen uptake just after feeding.
This, however, appeared to be due to activity stimulated
by feeding rather than feeding per se. Reasons for be-
lieving this are (1) the absence of a rise on the two days
when the animal was not active after feeding and (2) the
very short-term nature of the rise; it was over within an
hour or two of feeding. It should be noted, too, that the
peak at 10 days after capture occurred shortly before the
animal was fed rather than after. In the longer term there
is some indication that the average resting metabolic rate
is elevated by repeated feedings. During the period of daily
feedings on days 7-10 the resting rate rose to 0.6 mL:
kg~'-min™' and then declined to 0.3 mL:kg™!:min~! in
the three days fasting after this. Figure 2 shows the same
effect; animals tested 2-6 days after feeding take up oxygen
at only one-half to one-third of the rate of those tested
within 24 h of a meal.

DISCUSSION

Some of the results summarized above confirm statements
already made elsewhere. Thus, it is now quite certain,
despite some earlier doubts on the matter, that Nautilus
can regulate its oxygen uptake over a wide range of ambient
oxygen tensions.

The results following feeding were new and unexpected.
By analogy with Octopus vulgaris, another opportunistic
feeder, one might reasonably have expected a marked tran-
sient increase in oxygen uptake to follow the ingestion of
a meal. No such surge was seen. Very little is known about
digestion in Nautilus and nothing is published. The absence
of large salivary glands (which produce quantities of pro-
teolytic enzymes in coleoids), the small caecum, and the

M. J. Wells, 1987

1.0 ¢ N. pompilius

Page 73

@i

9 ® N. stenomphalus ;

8 ‘Hybrids’

O,
Consumption
ml Kg min"

Ss OG

ed

e414 g 8 ae
eZ @® 8.

@ 4 e 4
emis ee P18,
e e
. : ° Ok

1 weg Aeeealse:

1 1S

Leb Se Gs uid
TEMPERATURE C

Figure 2

Oxygen uptake and temperature in Nautilus. Metabolic rate increased rapidly with temperature. Figures against

outlying values show days since last fed.

unusual structure of the digestive gland (MANGOLD et al.,
in press) all suggest that digestion is rather different from
the system in coleoids (for review, see BOUCAUD-CAMON
& BOUCHER-RODONI, 1983). Two facts from the present
series of observations confirm the impression from the oxy-
gen uptake experiments, that digestion in Nautilus is prob-
ably rather slow. One is the amount that animals would
eat. All the individuals tested fed readily if presented with
dead fish or pieces of crab, but they never took more than
about 25 g of flesh. ZANN (1984) reported crop weights
averaging more than 50 g from smaller animals caught in
traps off Fiji. The implication is that the Lizard Island
animals, first tested within a few days of arrival, were still
“topping up” crops only part emptied after the last meal,
having gorged themselves to repletion in the traps. The
slow emptying of the crop was confirmed when animal
LZ19 was killed. This Nautilus had not been fed for 3

days (see Figure 3) but it still had crab remains in the
crop.

If digestion is as leisurely as these results suggest, it is
likely that the great majority of the oxygen consumption
figures that we have so far collected for Nautilus (REDMOND
et al., 1978; WELLS & WELLS, 1985, and in this account)
are typical of fed rather than fasted animals, because all
are derived from animals tested within a few days of cap-
ture in traps, where presumably, they gorged themselves.
By analogy with Octopus, one would expect the metabolic
rate to fall considerably in starvation. In view of the slow
growth rate of Nautilus compared with other cephalopods
(WARD, 1983) and the possible scarcity of catchable food
in the depths where Nautilus lives, the possibility that the
animal can cut its standard metabolic rate to low levels in
lean times is important to our understanding of its ecology.
The present series shows (Figures 2, 3) that oxygen uptake

Page 74

os
20) TL
oD)
(@)
Q
Lu
(LL,
1.5
O,
Consumption
-1 rl | O i ACTIVE
ml Kg min
ACTIVE
ACTIVE
Or5
0
4 5 6 i

reD Fh

The Veliger, Vol. 30, No. 1

LZVg

FED 136) GaVAs)

FED 7g CRAB
FED 24g CRAB

|} AFTER ACTIVITY

8 9 10 111 2 13

DAYS AFTER CAPTURE
Figure 3

Metabolic rate and feeding history of Nautilus pompilius LZ19, body weight 390 g. ‘“‘Active” means seen to be
jetting about its respirometer at one or more spot checks made during oxygen uptake runs. The animal still had
crab remains in the crop when killed 13 days after capture and 3 days after the last meal.

is reduced to one-half or even less by three days of fasting.
We need a much longer series of oxygen uptake experi-
ments to find out just how flexible Nautilus is in this respect.

Nautilus oxygen uptake is sensitive to temperature change
(Figure 2). The animal is known to move into shallower
water at night, with vertical changes of as much as 200 m
not uncommon on such occasions (WARD et al., 1984).
Given the steep temperature profiles found along reef slopes
(see, for example, WARD & MarTIN, 1980) and the lack
of time for temperature adaption during these excursions,
Nautilus is likely to be altering its standard metabolic rate
by a factor of two or three in daily cycles. We do not know
what part these changes may play in the economic strategy
of Nautilus, but it is conceivable that the animal is econ-
omizing by feeding during its nightly excursions into re-
gions of higher temperature and then dropping down to

the cooler deeps to digest, as young salmon, for instance,
are known to do in similar diurnal cycles (BRETT, 1983).

Given the information now available about oxygen con-
sumption at rest and in activity, the Q,. and vertical mi-
grations, temperature profiles off the reef face, and activity
patterns, it is possible to construct an elementary energy
budget for Nautilus. Crudely, with an oxygen uptake of
around 0.5 mL-kg~'-min“' at rest at 17°C and twice that
at 22°C, and the animal spending half of every 24 h at
each temperature (as indicated by records of vertical mi-
grations in WARD et al., 1984 and the temperature profiles
given in WARD & MarTIN, 1980) the likely oxygen con-
sumption over 24 h will be around 1080 mL-kg™'. To this
must be added the cost of locomotion, being the difference
between the active and resting oxygen consumptions, about
0.75 mL-kg~'-min~! (the cost of transport will not vary

M. J. Wells, 1987

significantly with temperature). Accepting ZANN’s (1984)
figures for the proportion of time spent actively swimming
(2.6 min:h~' during the day and 7 min-h~' at night, with
slightly higher figures at dawn and dusk) the added cost
of locomotion is around 110 mL:kg~'-day~'. Taking one
litre of oxygen to equal 4.6 kcal on a mainly protein diet
broken down to ammonia, and a value for fish flesh of 1.27
kcal-g~' wet weight (an average from values given in
WarTT, 1968), and 95% absorption of food ingested at a
cost of 0.04 kcal-g~' (as for Octopus, see O’DorR et al.,
1984), the daily requirement for a 500-g (flesh weight)
Nautilus would be around 2 g of fish. A cropfull would
keep the animal going for a month. This, it should be
remembered, is based on the metabolic rates of fed animals.
We know that the animal reduces its oxygen uptake by
50% after only three days of fasting. At this rate a square
meal might last for a couple of months assuming zero
growth but no loss of weight. Nautilus is evidently well
suited to a scavenging life-style and an irregular food sup-

ply.
LITERATURE CITED

BoucauD-Camou, E. & R. BOUCHER-RODONI. 1983. Feeding
and digestion in cephalopods. /n: A. S. M. Saleuddin & K.
M. Wilbur (eds.), The Mollusca, Vol. 5:149-187. Academic
Press: New York.

BRETT, J. R. 1983. Life energetics of the sockeye salmon,
Oncorhynchus nerka. In: W. P. Asprey & S. I. Lustick (eds.),
Behavioral energetics. Ohio State Univ. Press.

CARPENTER, J. H. 1966. New measurements of oxygen solu-

Page 75

bility in pure and natural waters. Limnol. Oceanogr. 11:
264-277.

JOHANSEN, K., J. R. REDMOND & G. B. BOURNE. 1978. Res-
piratory exchange and transport of oxygen in Nautilus pom-
pilus. Jour. Exp. Zool. 205:27-306.

MANGOLD, K., A. PORTMANN & A. M. BippeR. In press. Traité
de Zoologie. Grassé (ed.).

O’Dor, R. K., K. MANGOLD, R. BOUCHER-RODONI, M. J. WELLS
& J. WELLS. 1984. Nutrient absorption, storage and re-
mobilisation in Octopus vulgaris. Mar. Behav. Physiol. 11:
239-258.

REDMOND, J. R.,G. B. BOURNE & K. JOHANSEN. 1978. Oxygen
uptake by Nautilus pompilius. Jour. Exp. Zool. 205:45-50.

SAUNDERS, W. B. 1981. The species of living Nautzlus and their
distribution. Veliger 24:8-17.

WarbD, P. D. 1983. Nautilus macromphalus. In: P. R. Boyle
(ed.), Cephalopod life cycles, Vol. 1:11-28.

Warp, P. D., B. CARLSON, M. WEEKLY & B. BRUNBAUGH.
1984. Remote telemetry of daily vertical and horizontal
movement of Nautilus in Palau. Nature 309:248-250.

Warp, P. D. & A. W. MartTIN. 1980. Depth distribution of
Nautilus pompilius in Fiji and Nautilus macromphalus in New
Caledonia. Veliger 22:259-264.

Watt, B. K. 1968. Composition of foods, raw and processed.
Pp. 9-20. In: P. L. Altman & D. S. Dittmer (eds.), Metab-
olism. Fed. Amer. Soc. Exp. Biol.: Bethesda, Maryland.

WELLS, M. J., R. K. O’Dor, K. MANGOLD & J. WELLS. 1983.
Feeding and metabolic rate in Octopus. Mar. Behav. Physiol.
9:305-317.

WELLS, M. J. & J. WELLS. 1985. Ventilation and oxygen
uptake by Nautilus. Jour. Exp. Biol. 118:297-312.

ZANN, L. P. 1984. The rhythmic activity of Nautilus pompilius
with notes on its ecology and behavior in Fiji. Veliger 27:
19-28.

The Veliger 30(1):76-81 (July 1, 1987)

THE VELIGER
© CMS, Inc., 1987

The Indo-West Pacific Species of the Genus

Trigonostoma sensu stricto

(Gastropoda: Cancellariidae)

RICHARD E. PETIT ann M. G. HARASEWYCH

Department of Invertebrate Zoology, National Museum of Natural History,
Smithsonian Institution, Washington, D.C. 20560, U.S.A.

Abstract. Three Indo-West Pacific species referable to the nominotypical subgenus 777gonostoma are
compared and figured. 77rigonostoma antiquatum (Hinds, 1843) is shown to have been misidentified in
the literature, and 7. antzquatum of most authors other than Hinds is newly described herein. The three
Indo-West Pacific species recognized are: T7igonostoma scalare (Gmelin, 1791), 7. antiquatum (Hinds,

1843) and 7. thysthlon sp. nov.

INTRODUCTION

A study of the cancellariid subgenus 77:gonostoma s.s. in
the Indo-West Pacific reveals that there are three distinct
species. The species identified in the recent literature as
T. antiquatum (Hinds) is not that species, but a previously
unnamed species, described herein as 7. thysthlon sp. nov.
The lectotype of 7. antiquatum is figured, the first time it
has been illustrated photographically.

ABBREVIATIONS

Abbreviations for museum collections cited in this paper
are: AMNH, American Museum of Natural History, New
York; ANSP, Academy of Natural Sciences of Philadel-
phia; BM(NH), British Museum (Natural History), Lon-
don; MHNG, Muséum d’Histoire Naturelle, Genéve;
MNHN, Muséum National d’Histoire Naturelle, Paris;
NSMT, National Science Museum, Tokyo; USNM, Na-
tional Museum of Natural History, Washington.

SYSTEMATICS

Genus Trigonostoma Blainville, 1827

Trigonostoma BLAINVILLE, 1827:652.
Type species (monotypy) Delphinula trigonostoma La-
marck, 1822 [=Buccinum scalare Gmelin, 1791].
Trigona PERRY, 1811:pl. 51, non Trigona Jurin, 1807.

Subgenus 77zgonostoma s.s.

Trigonostoma scalare (Gmelin, 1791)

(Figures 1-3)

Buccinum scalare GMELIN, 1791:3495.
Trigona pellucida PERRY, 1811: pl. 51, figs. 1, 2.
Delphinula trigonostoma LAMARCK, 1822:231; BLAINVILLE,
1827:652; MERMOD & BINDER, 1963:170, fig. 234.
Cancellaria trigonostoma (Lamarck): DESHAYES, 1830:180;
SOWERBY, 1833:7, fig. 44; KIENER, 1841:41, pl. 1, fags.
1, la; DESHAYES, 1843:409; SOWERBY, 1849b:457, pl.
94, figs. 45, 46; REEVE, 1856, pl. 11, figs. 51a—b; TRYON,
1885:78, pl. 5, fig. 79; LOBBECKE, 1886:50, pl. 15, figs.
il, De

Trigonostoma pellucida (Perry): PETIT, 1967:217; ABBOTT &
DANCE, 1982:229 [figured].

Trigonostoma antiquata (Hinds): GARRARD, 1975:20, pl. 3,
fig. 16 [not of Hinds].

Trigonostoma trigonostoma (Deshayes): CHENU, 1859:276, fig.
1828; KIRTISINGHE, 1978:79, pl. 45, fig. 5.

Trigonostoma scalare (Gmelin): PETIT, 1984:58; VERHECKEN,
1986:59, fig. 27.

Diagnosis: Trigonostoma scalare may be readily distin-
guished from its congeners by its large size, concave sides,
and characteristic imbricate sculpture (Figure 3).

Range: Sri Lanka to the Philippines, southeast to northeast
Australia.

Remarks: The nomenclatural history of this distinctive
species has been given by PETIT (1984). GARRARD (1975:
20) misidentified the species as 7rigonostoma antiquata
(Hinds) and later (1983:6) considered 7. antiquata to be
a synonym of 7. trigonostoma, compounding his error by
attributing the latter name to “Linnaeus, 1758.”

R. E. Petit & M. G. Harasewych, 1987

Explanation of Figures 1 to 5

Figures 1, 2. Trigonostoma (Trigonostoma) scalare (Gmelin, 1791).
Figure 1. USNM 845609, taken by nets in 73 m, off Balut Is.,
Mindanao, Philippines. x 2.5.

Figure 2. Protoconch of specimen in Figure 1. x50.

Figure 3. Detail of surface sculpture of specimen in Figure 1.
x50.

Early locality citations for this species were given simply
as “Ceylon.” The Australian records given by GARRARD
(1975:21) cannot be accepted in their entirety owing to his
misidentification. However, his figured specimen (pl. 3,
fig. 16), definitely 77:gonostoma scalare, is stated to be from
“3 metres off Black Is., Whitsunday Group, Qld.” In the
past few years specimens have been taken from tangle nets

Figure 4. Trigonostoma (Trigonostoma) antiquatum (Hinds, 1843).
Detail of surface sculpture of paralectotype BM(NH) 1968416/
2, “Island of Corregidor, Manila Bay, Philippines.” x50.

Figure 5. Trigonostoma (Trigonostoma) thysthlon sp. nov. Detail
of surface sculpture of specimen in Figure 8. x 50.

off Bohol Island, central Philippines. VERHECKEN (1986:
59) reported a specimen from the Moluccas.

The location of the type of 7rigonostoma scalare is not
known. Gmelin based the name on an illustration in a
Meuschen sales catalog (see PETIT, 1984:58) and the dis-
position of that specimen is not known. The location of
the type of Perry’s 7. pellucida, stated to be in “Miss

Page 78 The Veliger, Vol. 30, No. 1

R. E. Petit & M. G. Harasewych, 1987

Mitford’s collection,” is also unknown. MERMOD & BINDER
(1963) described and figured the holotype of Delphinula
trigonostoma Lamarck, which is in MHNG.

Trigonostoma antiquatum (Hinds, 1843)
(Figures 4, 6, 7)

Cancellaria antiquata HINDS, 1843:49, 1844:43, pl. 12, figs.
77, tsi

Cancellaria antiquata Hinds: SOWERBY, 1849b:458, pl. 93,
fig. 27; REEVE, 1856, pl. 16, figs. 74a, b; TRYON, 1885:
79, pl. 5, fig. 88; LOBBECKE, 1886:57, pl. 16, figs. 9, 10.

Not Trigonostoma antiquatum (Hinds): HABE, 1961a:435, pl.
24, fig. 14; pl. 23, fig. 8; 1961b:73, pl. 36, fig. 8; LAN,
1980:95, pl. 41, figs. 93, 93a; ABBOTT & DANCE, 1982:
229 (all =T7. thysthlon sp. nov.).

Not Trgonostoma antiquata (Hinds): GARRARD, 1975:20, pl.
3, fig. 16 (=T. scalare (Gmelin, 1791)).

Trigonostoma antiquata (Hinds): VERHECKEN, 1986:60 (in
part).

Diagnosis: This species may be recognized by its smoothly
convex whorls as well as by the presence of about 9 evenly
spaced varices per whorl. Intervarical surface sculpture
(Figure 4) consists primarily of numerous spiral ridges of
irregular size.

Range: Along northern Indian Ocean to New Guinea.
Philippines?

Remarks: In his original description HINDs (1843) gave
the locality as “New Guinea; in twenty-two fathoms, coarse
sand.” He further stated that it had been “also observed
by Mr. Cuming at the island of Corregidor, Bay of Manila,
in seven fathoms, coarse sand.” The next year Hinds gave
only New Guinea as the habitat, not mentioning the Cum-
ing specimens. The Hinds material was not deposited in
the BM(NH) and its location is not known, leaving only
the Cuming specimens to serve as type material. The Brit-
ish Museum (Natural History) has the Cuming specimens
(BM(NH) 1968416) from which VERHECKEN (1986:60)
selected as lectotype BM(NH) 1968416/1 (Figure 6), the
remaining two specimens (1968416/2-3) becoming para-
lectotypes. The Philippine locality given for the Cuming
specimens is suspect, as additional specimens have not been

Page 79

Table 1

Trigonostoma (Trigonostoma) thysthlon sp. nov. Measure-
ments of shell characters. Linear measurements in mm.

is = S-

Character Mean SD Range
Shell length 20.0 2.6 16.3-23.7
Shell width 13.0 IES 10.9-15.6
Aperture length 8.0 1.0 6.4-9.5
pentane cog 0.40 0.01 0.39-0.42

Shell length

No. whorls, protoconch 195 0.19 1.75-2.25
No. whorls, teleoconch 5.0 0.22 4.75-5.2
Spire angle 60.7 4.9 54-69

found even though the Corregidor Island area has been
well collected. The possibility of incorrect locality data
cannot be ignored, especially as other Cuming material
stated to be from the Philippines, such as Cancellaria sem-
idisjuncta SOWERBY (1849a), has been shown to be from
localities far removed from the Philippines. All Philippine
specimens of 777gonostoma s.s. that have come to our at-
tention are assignable to either 7. scalare (Gmelin) or to
T. thysthlon sp. noy. described herein. VERHECKEN (1986:
60) cites 7. antiquatum as occurring in India, the Strait of
Hormuz, and the Gulf of Oman. We have examined sev-
eral additional specimens from the northwestern Indian
Ocean. These have regular varices and surface sculpture
characteristic of 7. antiquatum, although the shells tend to
be thinner and less convex.

Trigonostoma (Trigonostoma) thysthlon
Petit & Harasewych, sp. nov.

(Figures 5, 8-13, Table 1)

Description: Shell small, reaching 24 mm in height, coni-
spiral, deeply umbilicate. Protoconch (Figure 9) of 2 smooth
whorls, deflected slightly from coiling axis. Transition to
teleoconch delineated by fine lamellose varix with short
open spine at the shoulder followed by onset of spiral

Explanation of Figures 6 to 13

Figures 6, 7. Trigonostoma (Trigonostoma) antiquatum (Hinds,
1843).

Figure 6. Lectotype, BM(NH) 1968416/1, “Island of Corregi-
dor, Manila Bay, Philippines.” 2.5.

Figure 7. Protoconch of paralectotype BM(NH) 1968416/2. x50.
Figures 8-13. Trigonostoma (Trigonostoma) thysthlon sp. nov.

Figure 8. Holotype, USNM 747301, in 56-73 m, off west coast
of Wasir Is., West Wokam, Aru, Moluccas (5°30'S, 134°12’E).
2.5.

Figure 9. Protoconch of specimen in Figure 8. x50.

Figure 10. Paratype, Petit collection, in 15-20 m, Rio Cordo Del
Sur, Philippines. x 2.5.

Figure 11. Paratype, Petit collection, in 182 m, S of Makung Is.,
Taiwan. X2.5.

Figure 12. Paratype, NSMT 63633, in 90 m, off Wakayama
Prefecture, Japan. x 2.5.

Figure 13. Paratype, MNHN, in 143-178 m, off NW Mindoro,
Philippines (13°59’N, 120°14.5’E). x2.5.

Page 80

sculpture. Teleoconch with up to 6 tabulate whorls. Suture
deeply impressed. First 2 postnuclear whorls with 11 or
12 finely lamellose varices per whorl. Thereafter 11 or 12
open shoulder spines per whorl, varices absent. Two thick
varices in close apposition appear to mark the end of growth
in adult specimens. Surface sculpture (Figure 5) of inter-
secting axial and spiral elements, with the axial elements
being more prominent and consisting of fine, rounded rib-
lets. Spiral sculpture of numerous weak cords, each com-
posed of 2 or 3 fine threads. Aperture roughly triangular.
Siphonal canal very short, forming shallow indentation in
abapical corner of aperture. Outer lip of adult specimens
with 12-15 thin lirae between the double-varix, smooth
in subadults. Posterior portion of inner lip adpressed against
siphonal fasciole. Inner lip with 2 columellar and 1 si-
phonal folds. One additional columellar thread occasion-
ally occurring between the two columellar folds in large
adult specimens. Umbilicus deep, reaching protoconch.
Shell color white to pinkish brown. Aperture white. In-
ternal structure, periostracum, and soft parts unknown.

Holotype: USNM 747301, in 56-73 m, off west coast of
Wasir Island, West Wokam, Aru, Moluccas (5°30'S,
134°12'E), M. King Memorial Exp. sta. AWI 9P10, L =
16.5 mm.

Paratypes (8): Petit collection, in 15-20 m, Rio Cordo
Del Sur, Philippines, L = 21.9 mm; Petit collection, in
182 m, S of Makung Is., Taiwan, L = 24.2 mm; NSMT
63633, in 90 m, off Wakayama Prefecture, Japan, L =
19.3 mm, 20.7 mm; MNHN, in 143-178 m, off NW
Mindoro, Philippines (13°59'N, 120°14.5’E), L = 18.4
mm; ANSP 234758, in 90 m, Wakayama, Japan, L =
16.5 mm; AMNH 161104, off Kii Peninsula, Honshu,
Japan, L = 23.5 mm; AMNH 122818, off Kii, Honshu,
Japan, L = 16.5 mm.

Range: Southern Japan south to the Philippines.

Comparisons: This species most closely resembles 777-
gonostoma antiquatum from which it may be distinguished
by its lack of pronounced varices beyond the second post-
nuclear whorl. Its flat or slightly convex whorls further
distinguish it from 7. antiquatum which has rounded whorls.
The surface sculpture of 7. thysthlon consists of strong
axial and weaker spiral cords, while the surface sculpture
of 7. antiquatum consists of strong spiral and very weak
axial cords.

Etymology: From the Greek thysthlon, a torch carried in
the Bacchic festival.

ACKNOWLEDGMENTS

Mr. Donald Dan, West Friendship, Maryland, photo-
graphed numerous specimens of 77igonostoma in foreign
museums at our request. Dr. Akihiko Matsukuma, Na-
tional Science Museum, Tokyo, Dr. Robert Robertson,
Academy of Natural Sciences of Philadelphia, Dr. Phi-

The Veliger, Vol. 30, No. 1

lippe Bouchet, Muséum National d’Histoire Naturelle,
Paris, Dr. William K. Emerson, American Museum of
Natural History, New York, and Ms. Kathie Way, British
Museum (Natural History), London, all made available
material from their museums’ collections. Mr. Ron Par-
sons, Burlingame, California and Mr. P. W. Clover, Glen
Ellen, California, loaned specimens from their personal
collections. Mr. André Verhecken, Mortsel, Belgium, cor-
responded and furnished a photograph of 7. antiquatum
from the Strait of Hormuz. To all of the above we express
our appreciation for their assistance and cooperation.

LITERATURE CITED

AspBoTT, R. T. & S. P. DANCE. 1982. Compendium of seashells.
E. P. Dutton: New York. 411 pp.

BLAINVILLE, H. M. D. DE. 1825-1827. Manuel de malacologie
et de conchyliologie. Paris. Two Vols., 190 pls. [Text pp.
1-647 issued 1825; pp. 649-664 and plates issued 1827].

CHENU, J. C. 1859. Manuel de conchyliologie et de paleon-
tologie conchyliologique. Tome 1, pp. i-vii and 1-508, text-
figs. 1-3707. Paris.

DesHayEs, G. P. 1830. Encyclopédie méthodique. Histoire
Naturelle des Vers 2(1):1-256. Paris.

DEsHAYES, G. P. 1843. Histoire naturelle des animaux sans
vertebres. 2nd ed. Vol. 9. Paris. 725 pp.

GARRARD, T. A. 1975. A revision of Australian Cancellariidae
(Gastropoda: Mollusca). Rec. Austr. Mus. 30(1):1-62.
GARRARD, T. A. 1983. Notes on the family Cancellariidae.

Austr. Shell News (42):6.

GMELIN, J. F. 1791. Carolia Linné Systema Naturae per regna
tria naturae. Editio decima tertia. Vol. 1, Pt. 6 (Vermes):
3021-3910. Lipsiae.

Hase, T. 1961a. Coloured illustrations of the shells of Japan
(II). 148 pp., Appendix 42 pp., 66 pls. Osaka.

Haske, T. 1961b. Description of four new cancellariid species,
with a list of the Japanese species of the family Cancellar-
iidae. Venus 21(4):431-441, pls. 23, 24.

HInps, R. B. 1843. Description of ten new species of Cancel-
laria, from the collection of Sir Edward Belcher. Proc. Zool.
Soc. Lond. 11:47-49.

Hinps, R. B. 1844-45. The zoology of the voyage of H.M.S.
Sulphur. Mollusca, Pts. 1-3. London. 72 pp., 21 pls.
KIENER, L. C. 1841. Species général et iconographie des co-
quilles vivantes. Genre Cancellaire. Paris. 44 pp., 9 pls.
KIRTISINGHE, P. 1978. Sea shells of Sri Lanka. Charles E.

Tuttle Co.: Vermont. 202 pp., 61 pls.

LAMaARCK, J. B. P. A. 1822. Histoire naturelle des animaux
sans vertébres. Vol. 6(2):1-232. Paris.

LAN, T. C. 1980. Rare shells of Taiwan in color. Taipei. 144
pp., 63 pls.

LOBBECKE, T. 1881-87. Das genus Cancellaria. Systematisches
Conchylien-Cabinet von Martini und Chemnitz 4:1-108,
pls. 1-24.

MERMOD, G. & E. BINDER. 1963. Les types de la collection
Lamarck au Muséum de Genéve. Mollusques vivants. V.
Revue Suisse de Zoologie 70(7):127-172.

Perry, G. 1811. Conchology, or the natural history of shells;
containing a new arrangement of the genera and species. .. .
London. 4 pp., 61 pls. (with pl. expl.).

Petit, R. E. 1967. Notes on Cancellariidae (Mollusca: Gas-
tropoda). Tulane Stud. Geol. 5(4):217-219.

R. E. Petit & M. G. Harasewych, 1987

Petit, R. E. 1984. Some early names in Cancellariidae. Amer.
Malacol. Bull. 2:57-61.

REEVE, L. 1856. Conchologia iconica, 10, Cancellaria. London.
18 pls. (with pl. expl.).

Sowersy, G. B. 1832-33. The conchological illustrations. Can-
cellaria. Pts. 9-13. London. 5 pls. with explanations + cat-
alogue, 10 pp. [Pts. 9-12, figs. 1-35, published 1832; pt. 13,
figs. 36-44 and catalogue published 1833].

SOwERBY, G. B. 1849a. Descriptions of some new species of

Page 81

Cancellara in the collection of Mr. H. Cuming. Proc. Zool.
Soc. Lond. [for 1848] XV1(189):136-138.

SOWERBY, G. B. 1849b. Thesaurus conchyliorum. Cancellaria.
Pp. 439-461, pls. 92-96.

Tryon, G. W. 1885. Manual of conchology 7:65-98, pls. 1-
7. Philadelphia.

VERHECKEN, A. 1986. The Recent Cancellariidae of Indonesia

(Neogastropoda, Cancellariacea). Gloria Maris 25(2):29-
66.

The Veliger 30(1):82-89 (July 1, 1987)

THE VELIGER
© CMS, Inc., 1987

Two New Aeolid Nudibranchs from Southern California

DAVID W. BEHRENS

Pacific Gas and Electric Company, Biological Research Laboratory,
P.O. Box 117, Avila Beach, California 93424, U.S.A.

Abstract. Two species, Cuthona hamanni sp. nov

California are described.

INTRODUCTION

Southern California has historically been a very active area
for opisthobranch research. The vicinity of San Diego,
California, has produced numerous new species, as re-
cently as 1986: GOSLINER (1981) described Cuthona phoe-
nix and BERTSCH & OSUNA (1986) added T7itonia myra-
keenae. This paper describes the morphology of two new
aeolidacean nudibranchs belonging to the genera Cuthona
Alder & Hancock, 1855, and Eubranchus Forbes, 1938.

. and Eubranchus steinbecki sp. nov., from southern

TERGIPEDIDAE Thiele, 1931
Cuthona Alder & Hancock, 1855
Cuthona hamanm Behrens, sp. nov.
(Figures 1-5)
La Jolla aeolid (Cuthona sp.): BEHRENS, 1980:105, fig. 158.

Materials examined: (1) Holotype: one specimen ap-
proximately 9 mm long (preserved), collected intertidally

D. W. Behrens, 1987

Page 83

Figure |

Cuthona hamanmni Behrens, sp. nov. A. Living animal, 9-mm specimen collected from La Jolla, California. Pho-
tograph by Jeff Hamann. B. Living animal drawn from a color transparency. C. Detail of a ceras.

at La Jolla, California (32°51'N, 117°15’W) in July 1983
by Mr. Jeff Hamann. This specimen is deposited in the
collection of the California Academy of Sciences, Depart-
ment of Invertebrate Zoology and Geology (CAS), CASIZ
061410.

(2) Paratypes: two specimens, each 7 mm long (pre-
served) and collected concurrently with the holotype, are
also deposited in the CAS collection, CASIZ 061411.

(3) One specimen, 5 mm long (preserved), collected
intertidally at La Jolla, California, in May 1982 by Jeff

Hamann. This specimen is also deposited in the CAS
collection, CASIZ 061412. Color transparencies of living
Cuthona hamanni are on file at CAS.

Description: Living animals may reach 14 mm long. The
body is typically aeolidiform, elongate and graceful, ta-
pering posteriorly (Figure 1). The foot is narrow, linear,
tapering to a point posteriorly. The tail is long. The foot
corners are square and somewhat laterally produced. The
cephalic tentacles are cylindrical, tapering to a blunt point,

Page 84

ne an
EA §
Ces S ad g & S g
ce
go
Figure 2

Cuthona hamanni. Lateral view. an, anus; go, genital orifice; ne,
nephroproct.

and when extended to their fullest are equal in length to
the rhinophores. The rhinophores are closely set, long,
smooth, and tapering to a rounded tip. The cerata are
slightly clavate and attain a length equal to that of the
rhinophores (Figure 1C). In one specimen the ceratal half
formula was I 4, II 5 (pre-pericardial), III 5, IV 3, V 2,
VI 2 (post-pericardial). The ceratal arrangement is shown
in Figure 2. The anal pore is located immediately anterior
to the uppermost ceras of the first post-pericardial row, to
the right of the pericardial elevation (Figure 2). The neph-
roproct is just medial to the anal pore (Figure 2). The

The Veliger, Vol. 30, No. 1

genital orifice is located just below the pre-pericardial ce-
rata on the right side of the body (Figure 2).

The ground color of the body is transparent white. The
internal organs are easily seen through the body wall.
Irregular patches of white and dark-brown pigment occur
dorsally from the rhinophores to the tip of the tail. The
white patches are more laterally distributed than the brown
pigmentation. Some white spots occur on the head. The
distal ¥% of the rhinophores and cephalic tentacles is en-
crusted with white pigment, followed by a band of dark
brown more proximally. The remaining 3 is similar to
the ground color of the body. White speckling may overlay
the proximal % of these appendages. The coloration of the
cerata is complex (Figure 1B). The tip of each ceras is
white, followed by a granular appearing medial region.
The granular appearance of this region, which makes up
¥% the length of each ceras, is created by a series of uni-
formly spaced white specks overlaying the semi-translucent
liver diverticulum. The color of the liver varies from tan
to orange and salmon. Basally, the coloration of the liver
abruptly changes to kelly green, forming a characteristi-
cally dark band. Occasional brown specks were observed
on the cerata of several specimens.

The radular formula is 13-20 x 0.1.0. There are no

Figure 3

Cuthona hamanm. A. Scanning electron micrograph of radula. B. Drawing of a rachidian tooth.

D. W. Behrens, 1987

Page 85

Figure 4

Cuthona hamanni. A. Jaw. B. Masticatory border of the jaw.

preradular teeth. Each rachidian tooth is a tall horseshoe-
shaped arch, with a long articulatory socket on the anterior
surface on either side (Figures 3A, B). The central cusp is
barely differentiated from the denticles, but does form a
low ridge. There are 6 or 7 strong, equal-size denticles to
each side of the cusp. The jaws are lightly tinted gold and
broadly oval (Figure 4A). The masticatory border is short
and angular with 10 irregular denticles (Figure 4B).

The reproductive system is typically cuthonid (Figure
5). The penial papilla is conical, bearing a stylet, and is
associated with a large bulbous penial gland. The vas
deferens is prostatic. The receptaculum seminis comprises
a single lobe and inserts into a common junction at the
orifice of the large lobate female gland mass through a
short duct. The ampulla is bulbous and connects with the
receptaculum seminis through a long duct.

Discussion: Placement of Cuthona hamanni is based upon
the presence of a non-tapering radula and the absence of
a preradular tooth (GOSLINER & GRIFFITHS, 1981). The
presence of a penial stylet is variable within the genus
(MILLER, 1977).

Cuthona hamanni can be separated from northeastern
Pacific species by its distinctive body and ceratal coloration
and by the number of teeth in the radula. Pigmentation
on the body region in the form of opaque white patches
or spots occurs in C. abronia (MacFarland, 1966), C. al-
bocrusta (MacFarland, 1966), and C. perca (Marcus, 1958)
(McDONALD, 1983; BEHRENS, 1984). None of these species
bears white and brown patches of pigmentation simulta-
neously, however. The uniform spotting and the bold green
coloration of the liver diverticulum at the insertion of the
cerata differ strikingly from the ceratal coloration of all

Page 86

The Veliger, Vol. 30, No. 1

Pg

ee betsy
ey Mere

vd

Figure 5

Cuthona hamanni. Reproductive system. am, ampulla; fgm, female gland mass; pe, penis; pg, penial gland; rs,

receptaculum seminis; s, stylet; vd, vas deferens.

described species. The number of radular teeth in C. ha-
manni (13-20) is very low, approached only by C’ fulgens
(MacFarland, 1966), which has from 16 to 59 teeth, and
C. perca, bearing 16 to 35 radular teeth.

The specific name hamanni is chosen to acknowledge
the energetic and enthusiastic efforts of Mr. Jeff Hamann
to increase our knowledge of opisthobranch mollusks, not
only from southern California but throughout the world.
Jeffs collections of opisthobranch species, described and
undescribed, have assisted researchers in bringing many
fascinating discoveries to the attention of the scientific com-
munity as a whole. For myself and others, we thank him.

EUBRANCHIDAE Odhner, 1934
Eubranchus Forbes, 1938
Eubranchus steinbecki Behrens, sp. nov.
(Figures 6-9)
Eubranchus sp.: BEHRENS, 1980:105, fig. 157.

Material examined: (1) Holotype: one specimen approx-
imately 4 mm long (preserved) collected off boat floats at
Dana Landing, Mission Bay, San Diego, California
(32°42'N, 117°11’W) 18 August 1978 by Dr. T. M. Gos-
liner. This specimen is deposited in the collection of the
California Academy of Sciences, Department of Inverte-
brate Zoology and Geology (CAS), CASIZ 061413.

(2) Paratype: one specimen approximately 4 mm (pre-
served), collected intertidally at Palos Verdes, Los Angeles
County, California (34°00'N, 118°47’W) on 23 March
1985 by William Jaeckle. This specimen is also deposited

in the CAS collection, CASIZ 061414. Color transpar-
encies of a living Eubranchus steinbecki are on file at CAS.

Description: Living animals reach 6 mm long. The body
is typically aeolidiform (Figure 6). The foot is slightly
wider than the body, linear and tapering posteriorly into
a long tail. The foot corners are square. The cephalic
tentacles are cylindrical and short, about 1% the length of
the rhinophores (Figures 6, 7). The rhinophores are long,
smooth, and taper to a blunt tip. The cerata are cylindrical
and irregularly nodular (Figure 6B). The liver diverticu-
lum is nodular within each ceras. The cerata are arranged
in 6 or 7 oblique rows dorsolaterally on either side of the
dorsum. An example of the branchial half formula is I 2-
4, II 2-4 (pre-pericardial), HI 3-5, IV 3-4, V 2, VI 2
(post-pericardial). The largest cerata are dorsomedial, with
smaller ones situated marginally. The anal pore is anterior
to the medial ceras of the third row and ventral to the
pericardial elevation (Figure 7). The genital orifice lies
posteriorly to the first ceratal row on the right side (Figure
7).

The ground color of the body is tan with dark olive-
green mottling. The dark green pigmentation is concen-
trated dorsomedially, forming a series of longitudinal stripes
along the dorsum connecting the ceratal groups. This strip-
ing varies greatly, both in darkness and in width, depend-
ing on the specimen. The head and proximal regions of
the rhinophores and cephalic tentacles are speckled with
olive-green. There are wide lateral translucent areas around
the eyes. The rhinophores are tipped with white, followed
by a dark olive-green band. In some specimens a clear
band exists about 4 the length from the distal end, followed

D. W. Behrens, 1987

Page 87

Figure 6

Eubranchus steinbecki Behrens, sp. nov. A. Living animal. 4-mm specimen collected from Dana Landing. Photograph
by T. M. Gosliner. B. Living animal drawn from a color transparency.

by the speckled olive-green head color. The cephalic ten-
tacles are white tipped and may have a green—brown sub-
apical band. The cream-colored liver diverticulum is clear-
ly discernible in the cerata. The cnidosac is cream to white.
The cerata are covered with various amounts of dark green
specks that may disperse, forming rings around the nod-
ulations.

The buccal mass is muscular and the salivary glands
large. The radular formula is 73 x 1.1.1. The central cusp
of the rachidian tooth is set lower than the tips of the
adjacent denticles and forms a low, central ridge (Figure

8A). There are 4 strong denticles on each side of the central
cusp. The lateral teeth are thin rectangular plates with a
single cusp on the inner side (Figure 8B), and are typical
of the genus Ewbranchus. The basal leg of the lateral tooth
is long, and only slightly tapering, measuring 3 to 4 times
the height of the tooth. The jaws are narrow, tapering
posteriorly (Figure 8C). The masticatory border bears 19
or 20 denticles (Figure 8D).

The reproductive system is typically eubranchid (Figure
9). The hermaphroditic duct opens into the ampulla ter-
minally. There is a penial gland, and the penis bears an

Page 88

Figure 7

Eubranchus steinbecki. Lateral view. an, anus; go, genital orifice.

apparently cuticular stylet. The vas deferens is not pros-
tatic. The ovotestes bear about 12 acini. The region mid-
way between the small receptaculum seminis and the open-
ing of the vagina may function as a bursa copulatrix as
described in Eubranchus farrani (Alder & Hancock, 1844)
by EDMUNDs & KREss (1969:891, 897). The egg mass is
a white-colored coil of %4-% of a whorl attached to the
substrate at the center of the whorl. This mass is longer
than that described by Hurst (1967) for E. olwaceus
(O’Donoghue, 1922), but is similar in morphology to the
egg mass described for E. cucullus Behrens, 1985. Egg
masses collected 10 August 1976 at Dana Landing were

The Veliger, Vol. 30, No. 1

approximately 1 mm in diameter and were on the hydroid
Plumularia laganiforma.

Discussion: The characteristics delineating the genus Eu-
branchus are well defined (EDMUNDS & KREss, 1969).
BEHRENS (1985) summarized recent additions to this ge-
nus. Of the 28 species known world-wide, many bear green
pigmentation. Eubranchus doriae (Trinchese, 1874) from
the Mediterranean and Atlantic coasts of France is the
only other species to concentrate the dorsal pigmentation
to form two dark stripes connecting the ceratal groups.
Among the five west American species, the radular count
of 73 places E. stenbecki midway between E. cucullus
(82) and E. rustyus (Marcus, 1961) (50-60), with the
remaining species having fewer teeth (ROLLER, 1972;
McDonaLp, 1983). In this species also the central cusp
of the rachidian is shorter than the lateral cusps. Addi-
tionally, the number of denticles (19 or 20) on the mas-
ticatory border of the jaw of E. stewnbecki falls between
those of the above-mentioned species, with E. cucullus hav-
ing 25 and E. rustyus having 12-20 (ROLLER, 1972;
McDOona Lp, 1983).

The specific name steinbecki is chosen to give recog-
nition to the author and philosopher John Steinbeck (1902-

Ea

Figure 8

Eubranchus steinbecki. A. Rachidian tooth. B. Lateral tooth. C. Jaw. D. Masticatory border of the jaw.

D. W. Behrens, 1987

mg

Figure 9

Eubranchus steinbecki. Reproductive system. al, albumen gland;
am, ampulla; mg, mucus gland; ov, ovotestis; p, penis; pg, penial
gland; rs, receptaculum seminis; s, stylet; vd, vas deferens.

1969), the man who not only influenced the works of
Edward “Doc” Ricketts, but was himself so greatly influ-
enced by Doc that some have speculated that Steinbeck
may have joined the ranks of our colleagues had it not
been for Ricketts untimely death. Together they wrote The
Sea of Cortez and were nearing completion of The Outer
Shores (see HEDGPETH, 1978a, b).

ACKNOWLEDGMENTS

I would like to express my thanks to Jeff Hamann, Will
Jaeckle, and Terry Gosliner for providing me with the

Page 89

type material for these species, and to Jeff for his photo-
graph of Cuthona hamanni and to Terry for the scanning
electron micrograph and his photograph of Eubranchus
steinbecki.

LITERATURE CITED

BEHRENS, D. W. 1980. Pacific coast nudibranchs: a guide to
the opisthobranchs of the northeastern Pacific. Sea Chal-
lengers Inc.: Los Osos, Calif. 112 pp.

BEHRENS, D. W. 1984. Notes on the tergipedid nudibranchs
of the northeastern Pacific, with a description of a new species.
Veliger 27(1):65-71.

BEHRENS, D. W. 1985. A new species of Eubranchus Forbes,
1838, from the Sea of Cortez, Mexico. Veliger 28(2):175-
178.

BertscuH, H. & A. M. Osuna. 1986. A new species of 77ztonia
(Nudibranchia) from southern California and Baja Califor-
nia. Nautilus 100(2):46-49.

Epmunps, M. & A. Kress. 1969. On the European species of
Eubranchus (Mollusca: Opisthobranchia). Jour. Mar. Biol.
Assoc. U.K. 49:879-912.

GosLINER, T.M. 1981. A new species of tergipedid nudibranch
from the coast of California. Jour. Moll. Stud. 47:200-205.

GosLINER, T. M. & R. J. GRIFFITHS. 1981. Description and
revision of some South African aeolidacean Nudibranchia
(Mollusca, Gastropoda). Ann. S. Afr. Mus. 84(2):105-150.

HEDGPETH, J. W. (ed.) 1978a. The outer shores. Part 1. Ed
Ricketts and John Steinbeck explore the Pacific Coast. Mad
River Press Inc.: Eureka, Cal. 128 pp.

HeEDGPETH, J. W. (ed.) 1978b. The outer shores. Part 2.
Breaking through. Mad River Press Inc.: Eureka, Cal. 182
PP-

Hurst, A. 1967. The egg masses and veligers of thirty northeast
Pacific opisthobranchs. Veliger 9(3):255-288, 13 pls.
McDona.p, G. R. 1983. A review of the nudibranchs of the

California coast. Malacologia 24(1-2):114-276.

MILLER, M. C. 1977. Aeolid nudibranchs (Gastropoda: Opis-
thobranchia) of the family Tergipedidae from New Zealand
waters. Zool. Jour. Linn. Soc. 60(3):197-222.

ROLLER, R. A. 1972. Three new species of eolid Nudibranch
from the west coast of North America. Veliger 14(4):416-
423.

The Veliger 30(1):90-94 (July 1, 1987)

THE VELIGER
© CMS, Inc., 1987

First Records of the Pteropods Clio scheeler
(Munthe, 1888) and Clio andreae (Boas, 1886)

(Opisthobranchia: ‘Thecosomata) from

the Western Pacific Ocean

by

L. J. NEWMAN anpb J. G. GREENWOOD

Zoology Department, University of Queensland,
St. Lucia, Brisbane, Australia 4067

Abstract.

Single individuals of Clio andreae (=C. polita), taken in three oblique plankton hauls from

depths to 1000 m in the Coral Sea and Solomon Sea, are described and figured. This is the first published
record of the species from the Pacific Ocean. Three individuals of Clio scheele: similarly taken from
depths to 2000 m in the Coral Sea are also described and figured. This species was previously known

from a single individual captured off Patagonia.

INTRODUCTION

Thecosomatous pteropods are found in all oceans, being
most diverse in tropical waters and mainly epipelagic in
distribution (BE & GILMER, 1977). There have been few
studies of pteropods from waters off northeastern Australia
other than those arising from the “Siboga” (TEsCcH, 1904)
and “Challenger” (PELSENEER, 1888) expeditions, and from
the studies of RUSSELL & COLEMAN (1935), TESCH (1948),
‘TANAKA (1970), and SOLIS & WESTERNHAGEN (1978).

The present study arose from an examination of plank-
ton samples taken from depths in excess of 1000 m in
waters of the Coral Sea off northeastern Australia, and of
the Solomon Sea to the north of Australia. Amongst the
pteropods taken from those samples were two rare bath-
ypelagic forms, neither of which has previously been re-
corded from the western Pacific Ocean, and one of which
was previously known only from a single specimen taken
in the southeastern Pacific. The present paper describes
and illustrates western Pacific specimens of Clio scheelei
(Munthe, 1888) and Clio andreae (Boas, 1886), extending
greatly the known distribution ranges of both.

MATERIALS anp METHODS

All specimens were taken from plankton samples collected
from the Solomon Sea and Coral Sea in 1981-1982, pri-
marily for ichthyoplankton studies. Tows were made with
nets of 4.0-mm mesh through the water column from depths

greater than 1000 m to the surface. Samples were preserved
in 2-3% formalin and deposited in the Museum of Vic-
toria, Melbourne. Pteropods from those samples were made
available for the present study and all specimens examined
are lodged in the Museum of Victoria. Measurements were
made with the aid of Wild M5 and M20 microscopes.
Surface features were photographed using scanning elec-
tron microscopy (SEM). Thecate hydroids attached to the
protoconchs of both Clio andrea and C. scheelei were not
removed from our specimens prior to SEM treatment be-
cause of the extremely delicate nature of the shells. Thecate
hydroids also have been found attached to other thecosome
species (MILLARD, 1975). Only one of the three available
specimens of each species was subjected to SEM treatment
(and consequent damage). The best specimens were ex-
amined and drawn, but retained intact for museum de-
position. Radulae were extracted from the specimens prior
to the shell being subjected to SEM. The radula and buccal
tissue were left in 10% KOH for 24 h, stained in acid
fuchsin and prepared for light microscopy. Drawings were
made with the aid of a camera lucida.

Sample data and species occurrences are given in Ta-
ble 1.

RESULTS anp DISCUSSION
Clio andreae (Boas, 1886) (=C. polita Pelseener, 1888)

Single specimens of Clio andreae were taken in samples
from depths to greater than 1000 m at two stations in the

L. J. Newman & J. G. Greenwood, 1987

Page 91

Figure 1

Clo andreae, lateral view of shell specimen that measured 7.3 mm long, aperture width 3.4 mm maximum.

Coral Sea and one station in the Solomon Sea (see Table
1). The animals were intact but their shells were damaged.
All three specimens have been deposited in the Museum
of Victoria (reference No. F 53081-53083).

All our specimens showed good agreement with shell
features described by VAN DER SPOEL (1967, 1976) for
specimens of up to 14 mm in length and 7 mm in width.
The shell is transparent, fragile and colorless, and the
shape is long and slender. The surface is completely smooth
and without striae, but there is a protrusively rounded
lateral rib on each side (Figure 3D). These ribs extend to
the aperture rim, and are most prominent in the anterior
half of the body, diminishing more posteriorly and being
indiscernable in the posterior quarter (Figures 1, 3A-C).
The shell has a distinct dorsal curvature, this curvature
being more pronounced in the posterior third; the ventral
border is therefore convex. The protoconch is not uni-
formly rounded distally, having an oval shape with an
obtusely pointed distal end. The radula has 10 rows of
teeth, which is typical of the genus, the teeth being similar
in shape to those described for this species by VAN DER
SPOEL (1967).

Clio andreae is known to be bathypelagic, occurring in
depths below 1000 m. Populations are known to occur in
tropical, subtropical, and transitional waters of the North
and South Atlantic (VAN DER SPOEL, 1967, 1976). The
only previous record of this species from the Pacific Ocean
is contained in an unpublished report by McGowan (1960,
see BE & GILMER, 1977) who reported it from a depth of
135-250 m in the Gulf of Panama.

Clio scheele: (Munthe, 1888)

Single specimens were found in each of three samples
collected from the Coral Sea (see Table 1). In each case
the samples were taken by oblique hauls from a maximum
depth of approximately 2000 m. All three specimens were
found with the animal intact although some shell damage
was evident. All three specimens are deposited in the Mu-
seum of Victoria (reference No. F 53084-53086).

The shell is transparent, straight and slender, with the
surface annulated by equally spaced transverse lirations
(Figures 2, 3E-G). A lateral rib extends on each side from
the aperture rim to the protoconch; these ribs have a distinct

Table 1

Sample and shell data for occurrences of Clio andreae and C. scheelet.

Species & Sample
date no. Latitude Longitude

C. andreae

18 May 81 1007-3 6°40.1'S 150°32.8'E

1 Dec. 81 1043-5 12°21'S 146°30'E

2 Dec. 81 1046-8 12°38'S 148°55’E
C. scheelet

2 Dec. 81 1046-8 12°38'S 148°55’E

3 Dec. 81 1047-7 12°31'S 148°41'E

4 Dec. 81 1049-8 13°50'S 148°18’E

SEM indicates these specimens as photographed in Figure 3.

Shell dimensions (mm + 0.1)

Max. tow ime Aperture
depth (m) Start Finish Length width
? 0010 iy 12.6 5.1
1000 0105 0600 13.6 7.0
1450 1740 2355 7.3 3.4 (SEM)
1450 1740 2355 Specimen damaged
1650 0015 0635 8.9 4.3
2100 2400 0624 7.0 3.4 (SEM)

Page 92

0.05mm

Figure 2

B

The Veliger, Vol. 30, No. 1

A. Clio scheelei, dorsal view of shell specimen that measured 7.0 mm long, 3.3 mm aperture width. B. Portion of

radula showing median and marginal teeth.

median longitudinal indentation making them “gutter-
shaped” (Figure 3F, H). The protoconch is rounded and
separated from the teleoconch by a pronounced constriction.

The radula is composed of 10 rows of teeth. The lateral
teeth show spines on both margins and the median tooth
is bluntly pointed with fine serrations (Figure 2B).

Only one specimen of Clio scheelei has previously been
reported in the literature, and that was collected off the
coast of Patagonia (148°0'S, 77°0'W) near Cape Horn
(MUNTHE, 1888). This holotype cannot be located (van
der Spoel, personal communication). Munthe described
his specimen of C. scheele: as having a distinctive, broad
longitudinal “‘ridge”” widening towards the aperture. The
dorsal side of the shell was also described as having three
convex longitudinal ridges, the middle one being most pro-

nounced, but not being present on the posterior portion of
the shell. These broad ridges could not be discerned in our
Coral Sea specimens. However, because Munthe’s speci-
men was considerably larger than ours (being 16 mm in
shell length), it is possible that our specimens are at a
younger growth stage and that the formation of longitu-
dinal “ridges” only becomes evident as greater size is
achieved. In all other respects, our specimens agree with
MUNTHE’s (1888) original description of C. scheelei in:
having a straight shell shape; being dorsoventrally flat-
tened; having uniformly spaced transverse lirations; and
in having a distinct groove running lengthwise down the
center of the lateral ribs. Our specimens are therefore
attributed to that species.

Clio scheele: differs from all other Clio species in having

Figure 3

A-D, shell of Clio andreae: A, ventral view; B, lateral view; C, protoconch detail; D, detail of rounded lateral rib.
E-H, shell of Clio scheele: shell (damaged during SEM preparation): E, ventral view; F, lateral view; G, protoconch

detail; H, detail of indented lateral rib. Scale bars = 1 mm.

Page 94

a combination of the following shell characteristics: a
straight shell with a 2:1 length-to-width ratio, a distinct
constriction separating the protoconch and teleoconch, and
transverse surface liration. The only two species of Clio
that show any close similarity to C. scheele: are C. recurva
(Childern, 1823) and C. orthotheca (Tesch, 1948). TESCH
(1913) illustrated differences in shell shape between C.
scheelei and C. recurva. The shell of the latter is curved
ventrally at the posterior end, and its protoconch lacks a
constriction. Clio orthotheca has a shell that is straight in
shape, but does not have the distinctive liration as found
in C. scheeler. The only known record of C. orthotheca is
from the Indian Ocean (TESCH, 1948).

ACKNOWLEDGMENTS

Pteropod material was kindly made available by the Mu-
seum of Victoria. The study was funded by grants from
the 1984 Australian Biological Resource Study, and from
the University of Queensland. Mr. J. Hardy and Mr. R.
Grimmer, Electron Microscope Centre, University of
Queensland are thanked for their assistance. We also thank
Dr. S. van der Spoel and reviewers for their comments on
a draft of this paper.

LITERATURE CITED

Bg, A. W. H. & R. W. GILMER. 1977. A zoogeographic and
taxonomic review of euthecosomatous Pteropoda. Pp. 733-
808. In: A. T. S. Ramsey (ed.), Oceanic micropalaeontology,
Vol. 1. Academic Press: London.

Boas, J. E. V. 1886. Spolia Atlantica. Bidrag til Pteropodernes.
Morfologi og systematik samt til kundskaben om deres geo-

The Veliger, Vol. 30, No. 1

grafiske udbredelse. Vidensk. Selsk. Skr., 6 Raekke, natury-
idensk. mathemat. Afd. IV. I:1-231, pls. 1-8.

McGowan, J. A. 1960. The systematics, distribution and
abundance of Euthecosomata in the North Pacific. Doctoral
Thesis, Univ. California. 197 pp.

MiLiarD, N. A. H. 1975. Monograph of the Hydroida of
southern Africa. Ann. S. Afr. Mus. 68:215-216.

MUNTHE, H. 1888. Pteropoder i Upsala Universitets Zoolo-
giska Museum, samlade af Kapt. G. von Scheele. Bih. K.
Sv. Vet. Akad. Handlingar 13(4)(2):1-33.

PELSENEER, P. 1888. Report on the pteropods collected by
H.M.S. “Challenger” during the years 1873-1876. II. The
Thecosomata. Rep. Sci. Res. Voy. H.M.S. “Challenger”
during the years 1873-1876. Zoology, 23(i):1-132.

RUSSELL, F.S. & J. S. COLEMAN. 1935. The zooplankton IV.
The occurrence and seasonal distribution of the ‘Tunicata,
Mollusca and Coelenterata (Siphonophora). Sci. Rept. of the
Great Barrier Reef Exped. 1928-1929. 2(7):203-276.

Souis, N. B. & H. VON WESTERNHAGEN. 1978. Vertical dis-
tribution of euthecosomatous pteropods in the upper 100 m
of the Hilutangan channel, Cebu, The Philippines. Mar.
Biol. 48(1):79-87.

Tanaka, T. 1970. Geographical and vertical distribution of
Pteropoda and Heteropoda in the western Pacific. 2nd C.S.K.
Symposium, Tokyo, Sept. 1970.

TeEscH, J. J. 1904. The Thecosomata and Gymnosomata of
the Siboga Expedition. Siboga Rept. 52:1-92.

TescH, J. J. 1913. Pteropoda. Das Tierreich 36:1-154.

TESCH, J. J. 1948. The thecosomatous pteropods. II. The Indo-
Pacific. Dana Rept. 5(30):1-45.

VAN DER SPOEL, S. 1967. Euthecosomata. A group with re-
markable developmental stages (Gastropoda, Pteropoda). J.
Noorduijn en Zoon. N.V. Gorinchem. 375 pp.

VAN DER SPOEL, S. 1976. Pseudothecosomata, Gymnosomata
and Heteropoda (Gastropoda). Bohn, Scheltema and Hol-
kema: Utrecht. 484 pp.

The Veliger 30(1):95-101 (July 1, 1987)

THE VELIGER
© CMS, Inc., 1987

NOTES, INFORMATION & NEWS

Mass Mortality of the Bubble Snail Bulla gouldiana
Pilsbry, 1893 (Gastropoda: Opisthobranchia)
by
Timothy D. Stebbins
Department of Biological Sciences,
University of Southern California, and
Invertebrates Section,

Los Angeles County Museum of Natural History,
Los Angeles, California 90007, U.S.A.

Bulla gouldiana Pilsbry, 1893, is the largest of the Cali-
fornia bubble shells and ranges from Morro Bay, Cali-
fornia, to Ecuador (MCLEAN, 1978; BEEMAN & WILLIAMS,
1980). This snail is often very abundant in bays and la-
goons, and is one of the most common of all gastropods in
the Newport Bay and Mission Bay regions of southern
California (RICKETTS et al., 1985).

Mass mortality of Bulla gouldiana occurred following a
week of heavy rains during February 1986 in Morro Bay,
California, the northernmost extreme of this snail’s range.
Seventy-one percent of the B. gouldiana population (n =
283) was observed either dead or dying on the Morro Bay
mudflats during an intertidal survey (23 Feb. 1986; —0.3
m tide). The scattered remains of individuals without shells
were discovered at the higher tidal levels, while numerous
shelled specimens were observed dead or dying in the lower
tidal regions. Few snails appeared healthy and active.

It is unknown what caused this mass die-off of Bulla
gouldiana. The effects of an unidentified pathogen or fresh-
water are possible factors. A bacterial infestation may have
not only killed off much of the local B. gouldiana popu-
lation, but also rendered the animals unpalatable to local
predators and scavengers (Western Gulls and other shore-
birds did not appear to be feeding on the abundant snail
remains). Such disease outbreaks have been implicated in
catastrophic die-offs of shallow-water marine organisms
at other locations (see MENGE, 1979; DUNGAN et al., 1982).
The significant influx of freshwater resulting from severe
storm activity the week preceding the observations may
have caused the local mortality of B. gouldiana. Support
for this hypothesis is that nine dead or dying echiuran
worms, Urechis caupo Fisher & MacGinitie, 1928, were
also observed on the tidal flats. I have seen similar mortality
of U. caupo following heavy rains in Humboldt Bay, north-
ern California.

It is premature to determine the exact cause of the mass
mortality of Bulla gouldiana. Whatever the cause, several
other common mudflat invertebrates did not appear to be
affected. These included two other large opisthobranchs,
the predatory Navanax inermis (Cooper, 1862) and the
herbivorous Aplysia californica Cooper, 1863, as well as
the ghost shrimps Callianassa californiensis Dana, 1854,

and Upogebia pugettensis (Dana, 1852). It would be useful
to know whether similar mortalities of B. gouldiana have
occurred at other California locations following heavy storm
activity.

Acknowledgments

I thank R. C. Brusca, P. M. Delaney, R. S. Houston, and
several anonymous reviewers for comments on the manu-
script.

Literature Cited

BEEMAN, R. D. & G. C. WILLIAMS. 1980. Opisthobranchia
and Pulmonata: the sea slugs and allies. Pp. 308-354. In:
R. H. Morris, D. P. Abbott & E. C. Haderlie (eds.), In-
tertidal invertebrates of California. Stanford Univ. Press:
Stanford, Calif.

DuNGAN, M. L., T. E. MILLER & D. A. THOMSON. 1982.
Catastrophic decline of a top carnivore in the Gulf of Cal-
ifornia rocky intertidal zone. Science 216:989-991.

McLean, J. H. 1978. Marine shells of southern California.
Los Angeles Co. Mus. Natur. Hist., Sci. Ser. 24, Revised
edition: 1-104.

MENGE, B. A. 1979. Coexistence between the seastars Asterias
vulgaris and A. forbes: in heterogenous environment: a non-
equilibrium explanation. Oecologia 41:245-272.

RIckETTs, E. F., J. CALVIN & J. W. HEDGPETH, revised by D.
W. PHILLIPS. 1985. Between Pacific tides. 5th ed., Stanford
Univ. Press: Stanford, Calif. 652 pp.

“Punctum pusillum”
(Gastropoda: Pulmonata: Punctidae)—
a Correction
by
Barry Roth
Santa Barbara Museum of Natural History,
Santa Barbara, California 93105, U.S.A.

In two recent papers (ROTH, 1985, 1986), I introduced
the name Punctum (Toltecia) pusillum (Lowe, 1831) to the
literature of west North American land mollusks as a
senior synonym of Punctum conspectum (Bland, 1865).
This taxon has been recognized as a very widely dissem-
inated, “weedy” species that has received many names in
various parts of the world (GITTENBERGER et al., 1980;
GUNTRIP, 1986; ROTH, 1986). Its correct name, however,
is Paralaoma caputspinulae (Reeve, 1852).

The earliest name proposed is apparently Helix pusilla
Lowe (1831:46), based on specimens from Madeira. How-
ever, the combination Helix pusilla is at least twice preoc-
cupied and cannot be used for the species. VALLOT (1801:
5) described a Recent European land gastropod as H.
pusilla, as follows: “10. H. mignone. H. pusilla. Coquille

Page 96

globuleuse, legérement conique, a quatre spires; lévres sans
rebord.”’ Twenty-seven years later, FLEMING (1828:265)
described a Carboniferous fossil as Helix pusilla: “7. H.
pusilla.—Depressed, smooth, umbilicated, convex beneath.
Volutions round and tapering; their number about three.
Mouth roundish.—Mart. Pet. Derb. t. lii. f. 3.—In a fossil
pericarp, in Clay Ironstone, Derbyshire.”

Felix pusilla Lowe, 1831, is thus a junior primary hom-
onym of H. pusilla Vallot, 1801, and H. pusilla Fleming,
1828, and unavailable.

The earliest available name, as pointed out to me by
Dr. F. M. Climo of the National Museum of New Zea-
land, is evidently Helix caputspinulae Reeve, 1852, based
on specimens from New Zealand. Helix caputspinulae was
proposed in the explanatory text to a plate of Reeve’s
Conchologia Iconica dated at foot as “October 1851.” How-
ever, this plate is in the midst of a sequence of plates dating
from 1852, and the date 1851 is most likely a misprint.
The probable publication date is October 1852.

The original description of Helix caputspinulae cites
“Helix epsilon Pfeiffer, Pro. Zool. Soc. 1851” asa synonym.
Helix epsilon was first described in a paper (PFEIFFER,
1854) that, according to a collation of the Proceedings of
the Zoological Society of London (SCLATER, 1893), could
have been published no earlier than 22 March 1854.

The type species of Paralaoma Iredale, 1913, is P. raou-
lensis Iredale, 1913, from the Kermadec Island Group,
New Zealand, another synonym of P. caputspinulae, ac-
cording to CLIMO (1981). The type species of Toltecia
Pilsbry, 1926, is Thysanophora (Toltecia) jaliscoense Pils-
bry, 1926, which has most recently been considered
(PILSBRY, 1948) a subspecies of Punctum conspectum (i.e.,
Paralaoma caputspinulae). Toltecia is therefore a junior syn-
onym of Paralaoma. (It should be pointed out that our
anatomical knowledge of 7. jaliscoense is based on BAKER’s
(1927) dissections of specimens from Chapultepec Park,
Mexico, D.F., rather than on topotypes from Guadalajara,
Jalisco.)

Current practice is to rank Paralaoma as a genus of
Punctidae, rather than as a subgenus of Punctum; see, for
example, SMITH & KERSHAW (1979), CLIMO (1981), and
SOLEM & CLIMo (1985). The two genera apparently have
substantially different distributions and histories (F. M.
Climo, personal communication).

I am indebted to F. M. Climo and E. Gittenberger for
discussion of the synonymies involved in this case. Dr.
Gittenberger kindly supplied a photocopy of the scarce
Vallot reference.

Literature Cited

BAKER, H. B. 1927. Minute Mexican land snails. Proc. Acad.
Natur. Sci. Phila. 79:223-246, pls. 15-20.

Cuimo, F. M. 1981. Classification of New Zealand Arionacea
(Mollusca: Pulmonata). VIII. Notes on some charopid species,
with description of new taxa (Charopidae). Natl. Mus. New
Zealand Records 2:9-15.

The Veliger, Vol. 30, No. 1

FLEMING, J. 1828. A history of British animals. Bell & Brad-
fute: Edinburgh. 565 pp.

GITTENBERGER, E., H. P.M. G. MENKHOoRST & J. G. M. RAVEN.
1980. New data on four European terrestrial gastropods.
Basteria 44:11-16.

GuntTrip, D. W. 1986. Toltecia pusilla (Lowe, 1831) living in
Britain. Jour. Conchol. 32:200-201.

Lowe, R. T. 1831. Primitiae faunae et florae Maderae et
Portus-Sancti. Trans. Cambridge Philos. Soc. 4(1):1-70.

PFEIFFER, L. 1854. Descriptions of sixty-six new land shells,
from the collection of H. Cuming, Esq. Proc. Zool. Soc.
Lond. 20:56-70.

Pitssry, H. A. 1948. Land Mollusca of North America (north
of Mexico). Acad. Natur. Sci. Phila., Monogr. 3, 2(2):521-
UGS

REEVE, L. A. 1851-1854. Conchologia Iconica or, illustrations
of the shells of molluscous animals. Vol. VII. Containing a
monograph of the genus Helix. Pls. 1-62 (1851), 63-146
(1852), 147-174 (1853), 175-210, title p., index (1854).

Rotu, B. 1985. A new species of Punctum (Gastropoda: Pul-
monata: Punctidae) from the Klamath Mountains, Califor-
nia, and first Californian records of Planogyra clappi (Val-
loniidae). Malacol. Rev. 18:51-56.

RotH, B. 1986. Notes on three European land mollusks in-
troduced to California. Bull. So. Calif. Acad. Sci. 85:22-28.

SCLATER, P. L. 1893. List of the dates of delivery of the sheets
of the ‘Proceedings’ of the Zoological Society of London,
from the commencement of 1830 to 1859 inclusive. Proc.
Zool. Soc. Lond. (1893):435-440.

SHERBORN, C. D. 1902-1933. Index Animalium. C. J. Clay
& Sons: London. Sect. 1, 1195 pp., sect. 2, 7056 + 1098 pp.

SMITH, B. J. & R. C. KersHaw. 1979. Field guide to the non-
marine molluscs of south eastern Australia. Austral. Natl.
Univ. Press: Canberra. 285 pp.

SOLEM, A. & F. M. Ciimo. 1985. Structure and habitat cor-
relations of sympatric New Zealand land snail species. Mal-
acologia 26:1-30.

[VALLoT]. 1801. Exercice sur V’histoire naturelle. Ecole Cen-
trale du Département de la Céte-d’Or: Dijon. 8 pp. [SHER-
BORN (1902-1933) attributes authorship of this work to Val-
lot, but the latter’s name does not appear in the copy seen
by me, only (p. 8) the names of ten students who evidently
prepared the text as part of their studies at the Ecole Cen-
trale.]

Synonymy of Rabdotus sonorensis (Pilsbry, 1928) With
Rabdotus nigromontanus (Dall, 1897)
(Gastropoda: Pulmonata: Bulimulidae)
by
James E. Hoffman
Department of Ecology & Evolutionary Biology,
University of Arizona,

Tucson, Arizona 85721, U.S.A.

Rabdotus sonorensis (Pilsbry, 1928) was described from
shells collected by Francis C. Nichols, with the type locality
listed as “Copete Mine, near Carbo, Sonora, Mexico.”
The holotype (ANSP 142647a) and the paratypes (ANSP
142647) were deposited in the collection of the Academy
of Natural Sciences at Philadelphia.

PRATT (1974) stated that Rabdotus sonorensis was a syn-

Notes, Information & News

onym of R. nigromontanus (Dall, 1897), but gave no in-
formation about what basis was use for his synonymy.

In November of 1984, Walter B. Miller, Edna Naranjo
Garcia, and I made the first of several trips to the Carbo
area of Sonora, Mexico, in order to try to find the type
locality of Rabdotus sonorensis. Although we could find no
reference to Copete Mine on maps of the Carbo area, we
searched the localities of the abandoned mines near Carbo
for signs of R. nigromontanus or R. sonorensis, without
success. We also asked, in Carbo, whether anyone knew
of Copete Mine. One retired miner said that he had heard
of Copete Mine near the town of Rayon, Sonora; no one,
however, had knowledge of a Copete Mine in the vicinity
of Carbo. Rayon is approximately 60 km, by road, east of
Carbo.

After our return to Tucson from Carbo, Georganne
Fink, a colleague of ours, found a reference to Minas del
Copete on an old map of the Rayon area. Based upon
further study of old maps and our subsequent field work,
the locality of the Copete Mines is undoubtedly the type
locality of Rabdotus sonorensis. The mines are located ap-
proximately 17 km by road SSW of Rayon, in Cerro el
Cielo (29°37.3'N, 110°38.0’W) at an elevation of 700 m.

Our first expedition to the Copete Mines in November
1985 yielded many live adult Rabdotus bailey: (Dall, 1893),
and a number of Sonorella sitiens Pilsbry & Ferriss, 1915,
plus a few shells of R. sonorensis. Unfortunately, during
this trip we were not able to find a live R. sonorensis for
anatomical comparison with R. nigromontanus. The plants
at the locality include species of Jatropha, Bursera, Ceiba,
Stenocereus, Prosopis, Olnea, and several species of Acacia
including A. cymbispina.

During our second expedition to the mines in February
1986, we found the same species as before, except that Dr.
Miller found one live juvenile Rabdotus in leaf litter in a
north-facing rockslide approximately 5 km NNE of the
Copete Mines. After raising this snail to maturity, I dis-
sected it. Its shell is 15.9 mm high and 10.6 mm in diameter,
with 5.0 whorls; its penis is 10.2 mm, penile sheath 2.7
mm, epiphallus 2.4 mm, epiphallic cecum 4.0 mm, and
penial retractor muscle 1.9 mm in length—all within or
near the range of variation of R. nigromontanus, whose
shell measurements have varied from 15.4 to 18.8 mm
high, from 10.6 to 12.4 mm in diameter, and from 5.0 to
5.8 whorls, and whose range of measurement of repro-
ductive anatomies also largely encompasses those of the
above specimen (HOFFMAN, 1987). Additionally, the shells
from Cerro el Cielo and the surrounding area are within
the range of variation of R. nigromontanus, as are the shells
of the holotype and paratypes in the ANSP collection (a
photograph of the shell of R. sonorensis may be found in
PILsBRY, 1928; photographs of a typical R. nigromontanus
shell are located in HOFFMAN, 1987). Therefore, I confirm
Pratt’s conclusion that Rabdotus sonorensis (Pilsbry, 1928),
is a junior subjective synonym of Rabdotus nigromontanus
(Dall, 1897) and, accordingly, is not valid.

Page 97

Acknowledgments

I am indebted to Georganne Fink for locating Las Minas
del Copete and to her husband, Jim Fink, for providing
the map. I also acknowledge with pleasure the help of Dr.
Walter B. Miller and Edna Naranjo Garcia. They accom-
panied me on every trip to resolve this problem, and also
provided much helpful advice. Jane E. Deisler located the
type material for me in the collection of the Academy of
Natural Sciences at Philadelphia, for which I will always
be grateful.

Literature Cited

HorrMaN, J. E. 1987. A new species of Rabdotus (Gastropoda:
Pulmonata: Bulimulidae) from Sonora, with a description
of the reproductive anatomy of Rabdotus nigromontanus. Ve-
liger 29:419-423.

Pitssry, H. A. 1928. Mexican mollusks. Proc. Acad. Natur.
Sci. Phila. 80:115-117.

Pratt, W.L., JR. 1974. A revision of the mainland species of
the bulimulid land snail genus Rabdotus. Bull. Amer. Malac.
Union, Inc., for 1973:24-25.

Range Extension for Doridella steinbergae (Lance, 1962)
to Prince William Sound, Alaska
by
Nora R. Foster
University of Alaska Museum,
Fairbanks, Alaska 99775, U.S.A.

Doridella steinbergae (Lance, 1962) is a small nudibranch
found on colonies of the bryozoan Membranipora, which
encrusts fronds of the giant kelps Macrocystis pyrifera and
Nereocystis luetkiana. Its known range was given by MIL-
LEN (1983) as Bamfield, Vancouver Island, British Co-
lumbia (48°50'N) to Los Coronados Island, Baja Califor-
nia (30°25/N).

On 20 July 1986, I collected and examined a Nereocystis
luetkiana plant from Gibbon Anchorage, Green Island,
Prince William Sound (60°17'N, 147°25'W). Large col-
onies of a Membranipora tentatively identified as M. ser-
rilamella Osburn, 1950, were present, along with Doridella
steinbergae and its egg masses. The nudibranch was ex-
amined in the field with a hand lens. The shape and
pigmentation were compared with illustrations of D. stein-
bergae and Corambe pacifica MacFarland & O’Donoghue,
1929, in Between Pacific Tides (RICKETTS et al., 1985:144).
The preserved specimens were later compared with the
original description.

Three specimens of the nudibranch, measuring 7.75
mm, 8.0 mm, and 8.75 mm in length after preservation,
egg masses, and the bryozoan were collected and preserved
for the Aquatic Collection, University of Alaska Museum,
Fairbanks, Alaska. These are in the wet collection, acces-
sion number 1986-14.

Page 98

This range extension to the north and west is not sur-
prising because the small size and concealing color pattern
of this nudibranch make it easy to overlook. Doridella stein-
bergae seems likely to be present elsewhere along the south-
east and southcentral Alaskan coast where Nereocystis and
Macrocystis are common.

Acknowledgments

I thank Glenn Juday for the opportunity to participate in
the Green Island Research Natural Area survey, and Nan-
cy Lethcoe for a successful trip to Green Island.

Literature Cited

LANCE, J.R. 1962. A new Stiliger and a new Corambella (Mol-
lusca: Opisthobranchia) from the northwestern Pacific. Ve-
liger 5(1):33-38.

MILLEN, S. V. 1983. Range extensions of opisthobranchs in
the northeastern Pacific. Veliger 25(4):383-386.

RICKETTS, E. F., J. CALVIN & J. W. HEDGPETH, revised by D.
W. PHILLIPS. 1985. 5th ed. Between Pacific tides. Stanford
University Press: Stanford, Calif. 652 pp.

Hermaea vancouverensis O’ Donoghue, 1924, from
Kodiak Island and Unga Island, Alaska
by
Nora R. Foster
University of Alaska Museum,
Fairbanks, Alaska 99775, U.S.A.

Surveys of opisthobranch fauna from the northeastern Pa-
cific note the absence of sacoglossans from Alaskan waters
(MILLEN, 1980, 1983; LEE & FOSTER, 1985). Because of
their small size and seasonal occurrence, sacoglossans are
easily overlooked by collectors so that their occurrence in
Alaskan waters may be even more widespread than re-
corded here. This note is intended to remind workers of
the possible presence of these small gastropods in low
intertidal and shallow subtidal samples from Alaskan
waters.

Hermaea vancouverensis O’Donoghue, 1924, has been
identified from two southwestern Alaska localities: Hum-
boldt Harbor, between Popof and Unga islands, Shumagin
Islands (55°20.5'N, 160°32'W), and at Spruce Cape, Ko-
diak Island (57°47.25'N, 149°26.30'W).

The Humboldt Harbor sample was taken on 9 May
1985, using a pipe dredge in about 5 m of water, on a
sand and mud bottom with scattered large kelps (Agarum,
Laminaria). The sample was fixed in the field, then screened
and sorted at the University of Alaska Museum in Fair-
banks. Five specimens of Hermaea vancouverensis, ranging
in size from 2 to 4 mm, were found.

The Kodiak Island sample (12 Hermaea vancouverensis:
the largest 2 mm, the others less than 1 mm) was collected
23 May 1986 at Spruce Cape (57°47.25'N, 149°26.30’W)
at low tide in an exposed rocky setting. The animals were

The Veliger, Vol. 30, No. 1

associated with the alga Neoptilota sp. The epiphytic dia-
tom Isthmia nervosa, mentioned as a food item for H. van-
couverensis (WILLIAMS & GOSLINER, 1973), was abundant
on the alga.

The identification is based on characteristics of the rad-
ula, rhinophores, cerata, and pigmentation. Specimens are
in the Aquatic Collection, University of Alaska Museum,
accession numbers 1985-8 and 1986-8.

These observations extend the known range for this
species from Vancouver Island, British Columbia, the
northernmost locality given by MILLEN (1980). The ani-
mal has been found as far south as Bodega Head, Cali-
fornia. The semiprotected shallow benthic and exposed
rocky coast habitats reported here are similar to those
mentioned for the species by MILLEN (1980) and WIL-
LIAMS & GOSLINER (1973).

Acknowledgments

For their assistance in the field I thank Jim McCullough,
Alaska Department of Fish and Game, and Matthew Dick,
Kodiak Community College. Philip Lambert, British Co-
lumbia Provincial Museum, loaned specimens of sacoglos-
sans for comparison. Museum volunteers Jackie Herbert
and Dixie Ostlind screened and processed the samples.
Travel to Sand Point and Kodiak was made possible through
acquisition funds provided to the University of Alaska
Museum from the State of Alaska.

Literature Cited

LEE, R. S. & N. R. FosTer. 1985. A distributional list with
range extensions of the opisthobranch gastropods of Alaska.
Veliger 27(4):440-448.

MILLEN, S. 1980. Range extensions, new distribution sites, and
notes on the biology of sacoglossan opisthobranchs (Mol-
lusca: Gastropoda) in British Columbia. Can. Jour. Zoology
58(6):1207-1209.

MILLEN, S. 1983. Range extensions of opisthobranchs in the
northeastern Pacific. Veliger 25(4):383-385.

O’ DONOGHUE, C. A. 1924. Notes on the nudibranchiate Mol-
lusca from the Vancouver Island Region Part IV. Additional
species and records. Trans. Royal Can. Inst. 15(1):1-33, pls.
III.

WILLIAMS, G. C. & T. M. GosLiner. 1973. Range extensions
for four sacoglossan opisthobranchs from the coasts of Cal-
ifornia and the Gulf of California. Veliger 16(1):112-116.

Pinna rugosa Sowerby, 1835 (Bivalvia: Pinnidae)
at the Galapagos Islands
by
Yves Finet
Museum d’Histoire naturelle, Case postale 434,
CH-1211 Genéve 6, Switzerland

Distribution of the Species

Pinna rugosa Sowerby, 1835, is a pinnid bivalve occur-
ring through most of the Panamic marine province. How-

Notes, Information & News

ever, it has never been reported from the Galapagos Ar-
chipelago, nor from the other offshore islands of west
Central America, except from Clipperton Island.

The type locality of the species is the Island of Rey,
Panama, cited by SOWERBY (1835:34) as “Hab. in Sinu
Panamensi (Isle of Rey) . . . they were procured from sand
banks.”

Subsequently, several authors have given new records
for this species, extending its range from Baja California
to Panama (TOMLIN, 1928:190; PILsBRY & LOwE,
1932:140; Lowe, 1933:75; BALES, 1938:45; WILKINS,
1953:28; OLSSON, 1961:143; KEEN, 1958, 1971; plus other
literature cited in SALVAT & SALVAT, 1972).

In their study on the geographic distribution of Pinna
rugosa, SALVAT & SALVAT (1972) report it also from Clip-
perton Island, a Pacific island off Mexico. According to
the authors, although the species is known to occur in the
eastern Pacific throughout most of the Panamic marine
province, it is not known to occur on offshore islands like
Cocos Island or the Galapagos Islands; according to the
same authors, Clipperton seems to be “the only island with
representatives of the family Pinnidae or with Pinna ru-
gosa.”

Actually, other representatives of the family Pinnidae
are known to occur in the Galapagos, including Atrina
texta Hertlein, Hanna & Strong, 1943 (KEEN, 1971;
BERNARD, 1983; FINET, 1985) and Atrina tuberculosa
(Sowerby, 1835) (BERNARD, 1983).

The Galapagan New Records

During the F.N.R.S.-Belgian Expedition to the Gala-
pagos in 1984, several empty shells of Pinna rugosa were
collected or observed:

(1) One empty shell of a juvenile specimen was collected
with the aid of SCUBA by Miss Burns and Mr. Stu-
pakoff on 10 July 1984; locality is channel between
Baltra and Santa Cruz Island, little island midway in
channel, with mangroves; 3 m (10 feet), sandy bottom
with boulders; water temperature 22.2°C.

(2) A large single valve was given to us by Senor Nestor

Garate Coronel, a local resident who helped us ex-

tensively collecting on Santa Cruz Island. The spec-

imen was found at a depth of about 3 m at Tortuga

Bay, Santa Cruz Island.

Empty, but complete shells (two valves) are sold in

groceries of Puerto Ayora, Santa Cruz; all are reported

to be caught by fishermen near Tortuga Bay (southern
coast of Santa Cruz Island). In addition, many com-
plete but empty shells of P. rugosa can be seen hung
for decoration on the walls of several restaurants at

Puerto Ayora; these specimens are generally said to

be caught by local fishermen.

(3

wa

These new records from the Galapagos, although not
including live-collected specimens, add a species of bivalve
to the list of the marine mollusks previously known to

Page 99

occur in this archipelago. They also extend the range of
Pinna rugosa to another group of offshore islands in the
eastern Pacific.

Literature Cited

Bates, M. D. 1938. Marine collecting on the west coast of
Mexico. Nautilus 52(2):41-46.

BERNARD, F. R. 1983. Catalogue of the living Bivalvia of the
eastern Pacific Ocean: Bering Strait to Cape Horn. Canadian
Spec. Publ. Fish. Aquat. Sci. No. 61:102 pp. Ottawa.

FINET, Y. 1985. Preliminary faunal list of the marine mollusks
of the Galapagos Islands. Docums. Trav. Inst. R. Sci. Natur.
Belg. No. 20:50 pp.

KEEN, A.M. 1958. Sea shells of tropical west America. Stanford
Univ. Press: Stanford, Calif. xi + 624 pp.

KEEN, A. M. 1971. Sea shells of tropical west America: marine
mollusks from Baja California to Peru. Stanford Univ. Press:
Stanford, Calif. xiv + 1064 pp.

Lowe, H.N. 1933. The cruise of the “Petrel.” Nautilus 46(3):
73-76.

Oxsson, A. A. 1961. Mollusks of the tropical eastern Pacific,
particularly from the southern half of the Panama-Pacific
faunal Province (Panama to Peru). Panamic-Pacific Pelecy-
pods. Paleont. Res. Inst.: Ithaca, N.Y. 574 pp.

Pitspry, H. A. & H.N. Lowe. 1932. West Mexico and Central
American mollusks collected by H. N. Lowe, 1929-31. Proc.
Acad. Natur. Sci. Phila. 84:33-144.

SALVAT, B. & F. SALVAT. 1972. Geographic distribution of
Pinna rugosa Sowerby, 1835 (Mollusca: Bivalvia) and its
occurrence on Clipperton Island. Veliger 15(1):43-44.

Sowersy, G. B. 1835. [no title] Proc. Zool. Soc. Lond. 3:84.

ToMLIN, J. R. LE B. 1928. The Mollusca of the ‘St. George’
Expedition. Jour. Conch. Lond. 18(7):187-198.

WILkIns, G. L. 1953. Notes from the British Museum. I, Pinna.
Proc. Malacol. Soc. Lond. 30:23-29.

California Malacozoological Society

California Malacozoological Society, Inc., is a non-profit
educational corporation (Articles of Incorporation No.
463389 were filed 6 January 1964 in the office of the
Secretary of State). The Society publishes a scientific quar-
terly, The Veliger. Donations to the Society are used to
pay a part of the production costs and thus to keep the
subscription rate at a minimum. Donors may designate
the Fund to which their contribution is to be credited:
Operating Fund (available for current production); Sav-
ings Fund (available only for specified purposes, such as
publication of especially long and significant papers); or
Endowment Fund (the income from which is available.
The principal is irrevocably dedicated to scientific and
educational purposes). Unassigned donations will be used
according to greatest need.

Contributions to the C.M.S., Inc., are deductible by
donors as provided in section 170 of the Internal Revenue
Code (for Federal income tax purposes). Bequests, lega-
cies, gifts, and devises are deductible for Federal estate and
gift tax purposes under sections 2055, 2106, and 2522 of

Page 100

the Code. Upon request, the Treasurer of the C.M.S., Inc.,
will issue suitable receipts which may be used by donors
to substantiate their tax deductions.

Subscription Rates and Membership Dues

At its regular Annual Business Meeting on 23 September
1986, the Executive Board of the California Malacozoo-
logical Society, Inc., set the subscription rates and mem-
bership dues for Volume 30 of The Veliger. For affiliate
members of the Society, the subscription rate for Volume
30 will be US$25.00; this now zncludes postage to domestic
addresses. For libraries and nonmembers the subscription
rate will be US$50.00, also now with postage to domestic
addresses included. An additional US$3.50 is required for
all subscriptions sent to foreign addresses, including Can-
ada and Mexico.

Affiliate membership in the California Malacozoologi-
cal Society is open to persons (no institutional member-
ships) interested in any aspect of malacology. There is a
one-time membership fee of US$2.00, after payment of
which, membership is maintained in good standing by the
timely renewal of the subscription.

Send all business correspondence, including subscription
orders, membership applications, payments for them, and
changes of address to C.M.S., Inc., P.O. Box 9977, Berke-
ley, CA 94709.

Page Charges

Although we would like to publish papers without charge,
high costs of publication require that we ask authors to
defray a portion of the cost of publishing their papers in
The Veliger. We wish, however, to avoid possible financial
handicap to younger contributors, or others without fi-
nancial means, and to have charges fall most heavily on
those who can best afford them. Therefore, the following
voluntary charges have been adopted by the Executive
Board of the California Malacozoological Society: $30 per
printed page for authors with grant or institutional support
and $10 per page for authors who must pay from personal
funds (2.5 manuscript pages produce about 1 printed page).
In addition to page charges, authors of papers containing
an extraordinary number of tables and figures should ex-
pect to be billed for these excess tables and figures at cost.
It should be noted that even at the highest rate of $30 per
page the Society is subsidizing well over half of the pub-
lication cost of a paper. However, authors for whom the
regular page charges would present a financial handicap
should so state in a letter accompanying the original manu-
script. The letter will be considered an application to the
Society for a grant to cover necessary publication costs.
We emphasize that these are voluntary page charges and
that they are unrelated to acceptance or rejection of manu-
scripts for The Veliger. Acceptance is entirely on the basis
of merit of the manuscript, and charges are to be paid after

The Veliger, Vol. 30, No. 1

publication of the manuscript, if at all. Because these con-
tributions are voluntary, they may be considered by authors
as tax deductible donations to the Society. Such contri-
butions are necessary, however, for the continued good
financial health of the Society, and thus the continued
publication of The Veliger.

Reprints

While it was hoped at the “birth” of The Veliger that a
modest number of reprints could be supplied to authors
free of charge, this has not yet become possible. Reprints
are supplied to authors at cost, and requests for reprints
should be addressed directly to the authors concerned. The
Society does not maintain stocks of reprints and also cannot
undertake to forward requests for reprints to the author(s)
concerned.

Patronage Groups

Since the inception of The Veliger in 1958, many generous
people, organizations, and institutions have given our jour-
nal substantial support in the form of monetary donations,
either to The Veliger Endowment Fund, The Veliger Op-
erating Fund, or to be used at our discretion. This help
has been instrumental in maintaining the high quality of
the journal, especially in view of the rapidly rising costs
of production.

At a recent Executive Board Meeting, we felt we should
find a way to give much-deserved recognition to those past
and future donors who so evidently have our best interests
at heart. At the same time, we wish to broaden the basis
of financial support for The Veliger, and thus to serve our
purpose of fostering malacological research and publica-
tion. Accordingly, it was decided to publicly honor our
friends and donors. Henceforth, donors of $1000.00 or
more will automatically become known as Patrons of The
Veliger, donors of $500.00 or more will be known as Spon-
sors of The Veliger, and those giving $100.00 or more will
become Benefactors of The Veliger. Lesser donations are
also sincerely encouraged, and those donors will be known
as Friends of The Veliger. To recognize continuing support
from our benefactors, membership in a patronage category
is cumulative, and donors will be listed at the highest
applicable category. As a partial expression of our grati-
tude, the names only of donors in these different categories
will be listed in a regular issue of the journal. Of course,
we will honor the wishes of any donor who would like to
remain anonymous. The Treasurer of the California Mal-
acozoological Society will provide each donor of $10.00 or
more with a receipt that may be used for tax purposes.

We thank all past and future donors for their truly
helpful support and interest in the Society and The Veliger.
Through that support, donors participate directly and im-

Notes, Information & News

portantly in producing a journal of high quality, one of
which we all can be proud.

Notes to Prospective Authors

The increasing use of computers to prepare manuscript
copy prompts the following notes. We request that the
right margin of submitted papers be prepared “ragged,”
that is, not justified. Although right-justified margins on
printed copy sometimes look “neater,” the irregular spac-
ing that results between words makes the reviewer’s, ed-
itor’s, and printer’s tasks more difficult and subject to error.
Similarly, the automatic hyphenation capability of many
machines makes for additional editorial work and potential
confusion; it is best not to hyphenate words at the end of
a line. Above all, manuscripts should be printed with a
printer that yields unambiguous, high-quality copy. With
some printers, especially some of the dot-matrix kinds,
copy is generally difficult to read and, specifically, the
letters “a, p, g, and q” are difficult to distinguish, especially
when underlined as for scientific names; again, errors may
result.

Other reminders are (1) that three copies of everything
(figures, tables, and text) should be submitted to speed the
review process, and (2) absolutely everything should be
double-spaced, including tables, references, and figure leg-
ends.

Because The Veliger is an international journal, we oc-
casionally receive inquiries as to whether papers in lan-
guages other than English are acceptable. Our policy is
that manuscripts must be in English. In addition, authors
whose first language is other than English should seek the
assistance of a colleague who is fluent in English before
submitting a manuscript.

Moving?

If your address is changed it will be important to notify
us of the new address at least six weeks before the effective
date and not less than six weeks before our regular mailing
dates. Send notification to C.M.S., Inc., P.O. Box 9977,
Berkeley, CA 94709.

Because of a number of drastic changes in the regulations
affecting second class mailing, there is now a sizable charge
to us on the returned copies as well as for our remailing
to the new address. We are forced to ask our members and
subscribers for reimbursement of these charges:

change of address and re-mailing of a returned issue—
$5.00.

Page 101

Sale of C.M.S. Publications

All back volumes still in print, both paper-covered and
cloth-bound, are available only through “The Shell Cab-
inet,” 12991 Bristow Road, Nokesville, VA 22123. The
same applies to the supplements still in print, with certain
exceptions (see below). Prices of available items may be
obtained by applying to Mr. Morgan Breeden at the above
address.

Volumes 1 through 13, 24, 26, and 27 are out of print.

Supplements still available are: part 1 and part 2, sup-
plement to Volume 3, and supplements to Volumes 7, 11,
14, 15, and 16; these can be purchased from ‘““The Shell
Cabinet” only. Copies of the supplement to Volume 17
(“Growth rates, depth preference and ecological succession
of some sessile marine invertebrates in Monterey Harbor”
by E. C. Haderlie) may be obtained by applying to Dr.
E. C. Haderlie, U.S. Naval Post-Graduate School, Mon-
terey, CA 93940.

Some out-of-print editions of the publications of C.M.S.
prior to Volume 26 are available as microfiche reproduc-
tions through Mr. Steven J. Long. The microfiches are
available as negative films (printed matter appearing white
on black background), 105 mm x 148 mm, and can be
supplied immediately. The following is a list of items now
ready:

Volumes 1-6: $9.95 each.

Volumes 7-12: $12.95 each.

Supplement to Volume 6: $3.95; to Volume 18, $6.95.
Send orders to Mr. Steven J. Long, Shells and Sea Life,
1701 Hyland, Bayside, CA 95524.

Single copies of back issues of The Veliger still in print
are available exclusively from:

Conchylien Cabinet,
Grillparzerstrasse 22,
D-6200 Wiesbaden, BRD (West Germany).

International Commission on
Zoological Nomenclature

The following applications have been received by the Com-
mission and have been published in Vol. 43, Part 4, of the
Bulletin of Zoological Nomenclature (11 December 1986).
Comment or advice on them is welcomed and should be
sent % The British Museum (Natural History), Cromwell
Road, London, SW7 5BD, England. Comments will be
published in the Bulletin.

Case No. 2571. Belemnites paxillosa Lamarck, 1801 (Mol-
lusca, Coleoida): proposed suppression of both generic
and specific names.

The Veliger 30(1):102-104 (July 1, 1987)

THE VELIGER
© CMS, Inc., 1987

BOOKS, PERIODICALS & PAMPHLETS

North Atlantic Nudibranchs (Mollusca) Seen by
Henning Lemche with Additional Species from the
Mediterranean and the North East Pacific

by HANNE JusT & MALCOLM EDMUNDs. 1985. Ophelia
Publications: Marine Biological Laboratory, Helsinggr,
Denmark. Supplementum 2:170 pp.

While Dr. Lemche was the Curator of Mollusca at the
Zoological Museum, University of Copenhagen (1958-
1974), he produced excellent water-color paintings of most
of the opisthobranchs he was able to study alive. Dr.
Lemche’s intention was to compile a monograph of North
Atlantic opisthobranchs illustrated with his own water-
color plates of each species. Unfortunately, Dr. Lemche
passed away in 1977 before he could complete his mono-
graph. Mrs. Hanne Just was Dr. Lemche’s graduate stu-
dent at the time of his death; she has prepared Dr. Lemche’s
material for publication, including the selection of the most
suitable paintings. The Preface and Introduction of the
book describe very well the background history in pub-
lishing the book.

This publication presents the best of Henning Lemche’s
nudibranch drawings, beautifully reproduced in full color.
One must certainly admire his artistic abilities to portray
accurately such delicate, flamboyant, and polychromatic
animals.

Species from the North Atlantic, the Mediterranean,
and the northeast Pacific (near Friday Harbor, Washing-
ton) are illustrated. The 69 plates are excellent; 46 animals
are identified to species, 22 only to genus (e.g., T7ztonia sp.
A), and 4 are identified to family (e.g., Dorididae sp. A).
These were mainly the identifications by Dr. Lemche, and
Just and Edmunds wisely did not change them. The un-
identified species may represent color variations of species
illustrated or of other North Atlantic forms, or some may
well be new species. Detailed work and collection of ad-
ditional material are necessary to clarify their taxonomy.

Four species illustrated are not listed in the Table of
Contents (Doto eireana, Doto columbiana, Doto cinerea, and
Doris verrucosa). Many of the species illustrated are com-
pared anatomically with similar or related species. An
index would have given a helpful entry to these taxa.

The text accompanying each plate (written by H. Just
and M. Edmunds) includes collecting data on and descrip-
tion of the specimen illustrated, ecological information
(usually diet and spawn), known distribution, and com-
ments regarding the species. The text is informative and
very well referenced.

The Appendix is an annotated list of North Atlantic
opisthobranchs by Elizabeth Platts. Drawn from the lit-
erature, it indicates in tabular form the presence or absence
of each species within 14 distribution areas. It has dis-

cussions of problems under “Notes on the Species,” and
its own section of references.

The difficulties of establishing a taxonomy that reflects
phylogeny were underscored by this work. Dr. Lemche
described a large number of Doto species with subtle color
variations, each of which occurs on a highly specific food
item (illustrated differences in egg masses between some
species substantiates these decisions). Yet it is well known
that the coloration of some species can vary greatly (plate
39 shows a large red and a yellow and brown juvenile of
Armina lovent), often in response to diet (e.g., p. 122, Cu-
thona nana, and p. 144, Spurilla neapolitana).

This is a useful, enjoyable, and aesthetic publication.

Hans Bertsch

A Field Guide to Caribbean Reef Invertebrates

by NANcy SEFTON & STEVEN K. WEBSTER. 1986. Sea
Challengers: Monterey, California. 112 pp. $19.95 U.S.

On the front cover of this beautiful volume is a photo-
graph of the red-legged hermit crab Paguristes cadenati,
peering out of its gastropod shell. This picture sets the
mood and tone for this guide book: the authors invite us
to look closely at (and appreciate and understand) the
marvelous invertebrate denizens of the Caribbean coral
reefs.

Included in this brilliantly illustrated guide book are
brief descriptions and color photographs of 179 inverte-
brate species and 16 plant species. The emphasis (over
half the species in the book) is appropriately on sponges
and cnidarians, as these are the predominant animals that
SCUBA divers see in the Caribbean. The text for each
species includes scientific and common names, a terse de-
scription identifying the organism’s salient features, and
some comments on its natural history. Often, notes on
behavior, feeding, enemies, “noxious level,” or habitat are
given. Prefacing the main field guide portion of the text
are a useful glossary (regrettably omitting “sessile”), a
section on coral reef geology, taxonomy, zonation, repro-
duction, growth and feeding, and a brief introduction to
the major invertebrate phyla.

The text is informative, often including the authors’ own
observations. Typographical errors are pleasantly rare.
Although several congeneric species are separated, the lay-
out is attractive. The color reproduction is excellent.

Having carried a camera underwater several times, I
can attest that Sefton and Webster have published an im-
pressive assemblage of underwater photographs. Because
most of the animals are illustrated in their natural habitat,
many of the photographs present important biological in-

Books, Periodicals & Pamphlets

formation about the species, as well as identifying char-
acteristics. The camera angles and composition of some
pictures show the animal so realistically that the reader is
almost underwater looking at the animal!

I wish I could have had this reference with me on a
recent expedition to the Caribbean.

Hans Bertsch

The Littorinid Molluscs of Mangrove Forests in the
Indo-Pacific Region: The Genus Littoraria

by Davip G. REID. 1986. British Museum (Natural His-
tory): London. Publication No. 978:xv + 228 pp. Price:
35 pounds.

In this scholarly work, the taxonomy of the “‘Littorina
scabra” complex is revised. Twenty species, all assigned
here to the genus Littoraria, are recognized from mangrove
forests in the Indo-Pacific region. Provided for each species
are synonymies, descriptions of shell, radula, and repro-
ductive anatomy, as well as information on habitat and
geographical distribution. Included are descriptions of one
new subgenus, two new species, and one new subspecies.

Before the individual species accounts, an informative
general account of the genus and its relation to others in
the Littorinidae is provided, with sections on morpholog-
ical characters (shell and anatomical), habitat (including
zonation patterns), behavior, and biogeography. Features
most useful in defining species are emphasized: those of
the shell (sculpture, microsculpture, columellar form) and
reproductive anatomy (penis, sperm nurse cells, pallial
oviduct).

The volume is well written, with many superb line and
halftone illustrations (plus a color frontispiece showing
shell polymorphism). Much of interest to students of gas-
tropods is contained within its pages, and the volume well
deserves a place on the shelf.

D. W. Phillips

Seashells of Western Australia

by FRED E. WELLS & CLAYTON W. BRYCE. 1985. Western
Australian Museum, Francis Street, Perth, W. Australia
6000. 207 pp.; 74 color plates.

Halfway through this book I was ready to schedule a
flight to Western Australia. Rarely has shell collecting
been presented in such an appealing, informative way.
This book, based largely on collections of the Western
Australian Museum, presents many of the common species
of mollusks in Western Australia (and as the authors point
out, animals rarely respect state borders, making the book
useful as well in other regions of Australia).

After some introductory sections to acquaint the reader
with the basics of resource conservation, local climates, and
when and where to collect, the organization of the book is

Page 103

taxonomic, by class and family. For each family, given
information includes the scientific name of the family, com-
mon name(s), a line drawing of a representative specimen,
a brief description of the family and its biology, and, usu-
ally, references for further reading. For each species, a
color photograph is provided, along with the scientific name
(complete with author and date), maximum size, relative
availability, and geographic distribution.

Both the illustrations and the text bear the clear marks
of professionalism and craftsmanship. The splendid color
plates (671 subjects on 74 plates) are as beautiful as they
are informative, crisply printed on glossy paper. The text
is concise and scientifically rigorous, while remaining in-
teresting and fluid, not ponderous.

As a result, the authors have succeeded in the difficult
task of producing a book, apparently designed primarily
for the amateur, that is sure to please both the interested
lay person and the scientist. This book is a sparkling in-
vitation to shell collecting in Western Australia and to
malacology.

D. W. Phillips

It’s Easy to Say Crepidula! (kreh PID’ yu luh)

by JEAN M. CaTE & SELMA RASKIN. 1986. Pretty Penny
Press, P.O. Box 3890, Santa Monica, CA 90403. $19.95
plus shipping.

For those who have been intimidated by scientific names,
help has arrived. Here is a handbook on pronunciation of
scientific names of mollusks that is certain to be useful,
and reassuring. No longer will there be an excuse to say
“quahog clams” when it’s so easy, and to my ear more
pleasing, to say Mercenaria (mer’ sen AIR’ ee uh).

Included with the phonetic guide are a glossary of terms
frequently used in malacology, a brief selection of con-
chological references, and an index of common names.
These too will be of value to many.

The major constraints on utility of the book are the too
frequent use of “sensu lato” genera and a rather skimpy
general index. Combined, these can create some difficulties.
For example, as chance would have it, the first three names
I chose to look up were not found directly: Ceratostoma
foliatum was listed under Murex (s.1.), Collisella under Ac-
maea (s.l.), and Olivella under Oliva (s.1.). Nor were the
three chosen genera listed in the General Index, so that a
student having just used a key to identify a specimen as
Ceratostoma foliatum would be unlikely to find the pro-
nunciation of folatum. In addition, nowhere would be the
pronunciation of Ceratostoma, the name in which I, for
example, was actually interested. The inclusion of addi-
tional genera would increase the utility and facility of the
manual.

Despite these omissions, hopefully to be addressed by
future editions, this phonetic guide makes a valuable con-
tribution by encouraging the use of scientific names. Fur-

Page 104

thermore, although designed specifically for conchologists,
students in other fields may also find it useful—the Greek
and Latin word roots that are combined into the specific
epithets of mollusks are, of course, often the same as those
used for animals of other taxonomic groups.

D. W. Phillips

Biology and Distribution of Early
Juvenile Cephalopods

edited by K. MANGOLD & S. v. BOLETZKY. 1985. Vie et
Milieu 35(3/4):139-304. The volume, priced at 240 French
Francs, can be ordered directly from the Editorial Office,
Laboratoire Arago, Vie et Milieu, F-66650 Banyuls-sur-
Mer, France.

This volume on cephalopods contains the proceedings
of an international symposium organized by K. Mangold
and S. v. Boletzky in 1985. It is published as a special
issue of the journal Vie et Milieu, which as of Volume 37
will also bear the English “subtitle” of Life and Environ-

The Veliger, Vol. 30, No. 1

ment. The list of participants in the symposium reads much
like an international “who’s who” of cephalopod biology,
and readers are sure to find much of interest within the
21 papers (some of them notes).

D. W. Phillips

Isla de Gorgona

edited by HENRY VON PRAHL & MICHAEL ALBERICO.
1986. Banco Popular: Bogota, Colombia. 252 pp., illust.

This new book by scholars associated with the Univer-
sidad del Valle in Cali, Colombia, has a number of chapters
that will be of interest to invertebrate zoologists: echino-
derms (Raul Neira & Von Prahl), corals (Von Prahl),
zoogeography of corals, crustaceans, mollusks (with a
species list), and fish (Von Prahl), and the gastropod su-
perfamily Muricacea (Francisco Borrero, Rafael Con-
treras & Jaime Cantera).

Eugene Coan

Information for Contributors

Manuscripts

Manuscripts must be typed on white paper, 842” by 11”, and double-spaced throughout
(including references, figure legends, footnotes, and tables). If computer generated copy
is to be submitted, margins should be ragged right (7.e., not justified). To facilitate the
review process, manuscripts, including figures, should be submitted in triplicate. The
first mention in the text of the scientific name of a species should be accompanied by the
taxonomic authority, including the year, if possible. Underline scientific names and other
words to be printed in italics. Metric and Celsius units are to be used.

The sequence of manuscript components should be as follows in most cases: title page,
abstract, introduction, materials and methods, results, discussion, acknowledgments, lit-
erature cited, figure legends, figures, footnotes, and tables. The title page should be on a
separate sheet and should include the title, author’s name, and address. The abstract
should describe in the briefest possible way (normally less than 200 words) the scope,
main results, and conclusions of the paper.

Literature cited

References in the text should be given by the name of the author(s) followed by the
date of publication: for one author (Smith, 1951), for two authors (Smith & Jones, 1952),
and for more than two (Smith ef al., 1953).

The “literature cited” section must include all (but not additional) references quoted
in the text. References should be listed in alphabetical order and typed on sheets separate
from the text. Each citation must be complete and in the following form:

a) Periodicals
Cate, J. M. 1962. On the identifications of five Pacific Mitra. Veliger 4:132-134.

b) Books
Yonge, C. M. & T. E. Thompson. 1976. Living marine molluscs. Collins: London.
288 pp.

c) Composite works

Feder, H. M. 1980. Asteroidea: the sea stars. Pp. 117-135. In: R. H. Morris, D. P.
Abbott & E. C. Haderlie (eds.), Intertidal invertebrates of California. Stanford Univ.
Press: Stanford, Calif.

Tables
Tables must be numbered and each typed on a separate sheet. Each table should be
headed by a brief legend.

Figures and plates

Figures must be carefully prepared and should be submitted ready for publication.
Each should have a short legend, listed on a sheet following the literature cited.

Text figures should be in black ink and completely lettered. Keep in mind page format
and column size when designing figures.

Photographs for half-tone plates must be of good quality. They should be trimmed off
squarely, arranged into plates, and mounted on suitable drawing board. Where necessary,
a scale should be put on the actual figure. Preferably, photographs should be in the
desired final size.

It is the author’s responsibility that lettering is legible after final reduction (if any)
and that lettering size is appropriate to the figure. Charges will be made for necessary
alterations.

Processing of manuscripts

Upon receipt each manuscript is critically evaluated by at least two referees. Based on
these evaluations the editor decides on acceptance or rejection. Acceptable manuscripts
are returned to the author for consideration of comments and criticisms, and a finalized
manuscript is sent to press. The author will receive from the printer two sets of proofs,
which should be corrected carefully for printing errors. At this stage, stylistic changes
are no longer appropriate, and changes other than the correction of printing errors will
be charged to the author at cost. One set of corrected proofs should be returned to the
editor.

An order form for the purchase of reprints will accompany proofs. If reprints are
desired, they are to be ordered directly from the printer.

Send manuscripts, proofs, and correspondence regarding editorial matters to: Dr. David W.

Phillips, Editor, 2410 Oakenshield Road, Davis, CA 95616 USA.

CONTENTS — Continued

The Indo-West Pacific species of the genus 777gonostoma sensu stricto (Gastrop-
oda: Cancellariidae).
RICHARD: BE. PET, AND) Mi'@SEYARASEWNCH) (75) ee ae ere

Two new aeolid nudibranchs from southern California.
IDAVID"' Wi sBEHIRENS = Tho Seay cee yr ao UTE ECR een Og

First records of the pteropods Clio scheeler (Munthe, 1888) and Clio andreae
(Boas, 1886) (Opisthobranchia: Thecosomata) from the western Pacific
Ocean.

Lic NEWMAN:AND J /G. (GREENWOOD! 92 cco8) faethe ied ets aaa

NOTES, INFORMATION & NEWS

Mass mortality of the bubble snail Bulla gouldiana Pilsbry, 1893 (Gastropoda:
Opisthobranchia).
TIMOTHY: DD. STEBBINS) '2.. 3, cee oe pee Re RS aE eae

“Punctum pusillum” (Gastropoda: Pulmonata: Punctidae)—a correction.
BARRY (RODHIS fai a: 028 ay ae) seer eee Cee Ec gee ann od

Synonymy of Rabdotus sonorensis (Pilsbry, 1928) with Rabdotus nigromontanus
(Dall, 1897) (Gastropoda: Pulmonata: Bulimulidae)
JAMES(E, (BIOPEMIANT (2122 5 Nese ete eeamte nent: eas naan ee sae eee

Range extension for Doridella stenbergae (Lance, 1962) to Prince William
Sound, Alaska.
INORA: R:, FOSTER! 2 02 oan at as, Need eh aed Seer

Hermaea vancouverensis O’ Donoghue, 1924, from Kodiak Island and Unga
Island, Alaska.
INGRAURE SBOSTERE i. 2. U2 = Ae ete eg ba ops 200 7 On oe

Pinna rugosa Sowerby, 1835 (Bivalvia: Pinnidae) at the Galapagos Islands.
YVESVRINE Dy ayes? sust bas: ot cals, eg til etras hea B: Syre Galan eee 0a ge a a

BOOKS| RERIO@ DIG ATES rea PAIV AIDE EI Sea eee

ISSN 0042-3211

( THE
VELIGER

A Quarterly published by

CALIFORNIA MALACOZOOLOGICAL SOCIETY, INC.

Berkeley, California

R. Stohler, Founding Editor \ OCT 1° 1987
\

Volume 30 - Ee Number 2
| a SIR eve mehr ni
CONTENTS By
Qh Deep-sea gastropods of the genus Aforia (Turridae) of the Pacific: species com-
401 position, systematics, and functional morphology of the digestive system.
Vax (MEN EE SYS OEVCAN DONG ICANTOR Wit yal o2 tie che a ly wha aici andl ae all coe Uae 105

MOLL
The effects of aggregation and microhabitat on desiccation and body temperature
of the black turban snail, Tegula funebralis (A. Adams, 1855).
IWARENU Eee MARCHED DIAND S| ONATHANGB . GEEVER 2 ))2)2. 2 i ts ss ee 127

Behavioral control of water loss in the terrestrial slug Deroceras reticulatum
(Miller): body-size constraints.
BIREAONIAS Ata NATE ties MA sere susie Sos Ria eke el Ahly Beer ks Uk cm 134

Responses of a mussel to shell-boring snails: defensive behavior in Mytilus edulis?
BIBEL@NVASDACMV AWN ie ta wh Manatee Si A NM Soe oe Bue ai elite 138

Skeletal growth histories of Protothaca staminea (Conrad) and Protothaca grata
(Say) throughout their geographic ranges, northeastern Pacific.
NOB ERI) Pe LARRIN GO Nie h en ae on ie nie MeL AAC Ee sk bs 3 eit 148

Age and growth of the subantarctic limpet Nacella (Patinigera) magellanica
magellanica (Gmelin, 1791) from the Strait of Magellan, Chile.
EONAR DOPEE; GUZMAN SAND! GARTOS: Ee RIOS)) 2ac).50 5c: 266 = Heese oe 1159

Herbivory in juvenile //yanassa obsoleta (Neogastropoda).
Cl ANIDE MASH RIEIN © EUIBENVG tah paiey ear eciiner iy alho: Saki Aayad (eae Aor Blane) 8 GS ap sine de fee ar 167

Starvation metabolism in the cerithiids Cerithidea (Cerithideopsilla) cingulata
(Gmelin) and Cerithium coralium Kiener.
Y. PRABHAKARA Rao, V. UMA DEvI, AND D. G. V. PRASADA RAO ....... NAS

CONTENTS — Continued

The Veliger (ISSN 0042-3211) is published quarterly on the first day of July, October,
January and April. Rates for Volume 29 are $25.00 for affiliate members (includ-
ing domestic mailing charges) and $50.00 for libraries and nonmembers (including
domestic mailing charges). An additional $3.50 is required for all subscriptions sent
to foreign addresses, including Canada and Mexico. Further membership and sub-
scription information appears on the inside cover. The Veliger is published by the
California Malacozoological Society, Inc., % Department of Zoology, University of
California, Berkeley, CA 94720. Second Class postage paid at Berkeley, CA and
additional mailing offices. POSTMASTER: Send address changes to C.M.S., Inc.,
P.O. Box 9977, Berkeley, CA 94709.

THE VELIGER

Scope of the journal
The Veliger is open to original papers pertaining to any problem concerned with mol-
lusks.

This is meant to make facilities available for publication of original articles from a
wide field of endeavor. Papers dealing with anatomical, cytological, distributional, eco-
logical, histological, morphological, physiological, taxonomic, etc., aspects of marine,
freshwater, or terrestrial mollusks from any region will be considered. Short articles
containing descriptions of new species or lesser taxa will be given preferential treatment
in the speed of publication provided that arrangements have been made by the author
for depositing the holotype with a recognized public Museum. Museum numbers of the
type specimen must be included in the manuscript. Type localities must be defined as
accurately as possible, with geographical longitudes and latitudes added.

Very short papers, generally not exceeding 500 words, will be published in a column
entitled “NOTES, INFORMATION & NEWS”; in this column will also appear notices
of meetings, as well as news items that are deemed of interest to our subscribers in
general.

Editor-in-Chief
David W. Phillips, 2410 Oakenshield Road, Davis, CA 95616, USA

Editorial Board

Hans Bertsch, National University, Inglewood, California

James T. Carlton, University of Oregon

Eugene V. Coan, Research Associate, California Academy of Sciences, San Francisco
J. Wyatt Durham, University of California, Berkeley

Terrence M. Gosliner, California Academy of Sciences, San Francisco
Cadet Hand, University of California, Berkeley

Carole S. Hickman, University of California, Berkeley

David R. Lindberg, University of California, Berkeley

James H. McLean, Los Angeles County Museum of Natural History
Frank A. Pitelka, University of California, Berkeley

Peter U. Rodda, California Academy of Sciences, San Francisco

Clyde F. E. Roper, National Museum of Natural History, Washington
Barry Roth, Santa Barbara Museum of Natural History

Judith Terry Smith, Stanford University

Ralph I. Smith, University of California, Berkeley

Wayne P. Sousa, University of California, Berkeley

T. E. Thompson, University of Bristol, England

Membership and Subscription
Affiliate membership in the California Malacozoological Society is open to persons (no
institutional memberships) interested in any aspect of malacology. As an affiliate member,
a person may subscribe to The Veliger for US $25.00, which now includes mailing
charges to domestic addresses. There is a one-time membership fee of US $2.00, after
payment of which, membership is maintained in good standing by the timely renewal of
the subscription; a reinstatement fee of US $3.00 will be required if membership renewals
do not reach the Society on or before April 1 preceding the start of the new Volume. If
a receipt is required, a self-addressed, stamped envelope (or in the case of foreign mem-
bers, the envelope and two International Postal Reply coupons) should be included with
the membership or subscription request.

The annual subscription rate to The Veliger for libraries and nonmembers is US
$50.00, which now includes mailing charges to domestic addresses.

An additional US $3.50 is required for all subscriptions sent to foreign addresses,
including Canada and Mexico.

Memberships and subscriptions are by Volume only (July 1 to April 1) and are payable
in advance to California Malacozoological Society, Inc. Single copies of an issue are US
$25.00 plus postage.

Send all business correspondence, including subscription orders, membership applications,
payments for them, changes of address, to: C.M.S., Inc., Post Office Box 9977, Berkeley,
CA 94709, USA.

Send manuscripts, proofs, books for review, and correspondence regarding editorial matters

to: Dr. David W. Phillips, Editor, 2410 Oakenshield Road, Davis, CA 95616, USA.

The Veliger 30(2):105-126 (October 1, 1987)

THE VELIGER
© CMS, Inc., 1987

Deep-Sea Gastropods of the Genus Aforia (Turridae) of

the Pacific: Species Composition, Systematics, and

Functional Morphology of the Digestive System
by

A. V. SYSOEV AND Yu. I. KANTOR

A. N. Severtzov Institute of Animal Evolutionary Morphology and Ecology of the U.S.S.R. Academy of Sciences,

Lenin Avenue, 33, Moscow 117071, U.S.S.R.

Abstract. The composition and distribution of deep-sea species of the genus Aforza from the Pacific
are studied. Three new subgenera, Dallaforia, Abyssaforia and Palaeoaforia, are described. Steiraxis
is considered as a taxon of the subgeneric level within Aforia. Three new species (Aforia abyssalis, A.
moskalevi and A. kupriyanovi) and one new subspecies (A. aulaca alaskana) are described.

The anatomies of seven species of Aforia, including the type species, are presented. On the whole, the
structure of all main organ systems is similar in most of the species. None of the species has an invaginable
part of the rhynchodaeum. It is shown that Toxoglossa possess an intraembolic proboscis characterized
by a buccal mass situated near its base.

An explanation is proposed of the feeding mechanism in turrids having a well-developed subradular
membrane and “nontoxoglossate” radular teeth. The explanation is based on findings of marginal teeth
held by a sphincter of the tip of the proboscis of Aforia species. Thus, marginal teeth perform a double
function, being used both in the buccal cavity and at the tip of the proboscis as in the higher Toxoglossa.

An analysis of the geographical distribution and history of members of Aforza shows that the main

factor conditioning the evolution of the genus is its adaptation to low water temperatures.

INTRODUCTION

Gastropods of the genus Aforza are among the largest (adult
shell sizes up to 92 mm) and most widely distributed
members of the family Turridae in the Pacific. Species of
Aforia are mostly found in relatively deep waters, and
descriptions of the specific composition of Aforia in bathyal
and abyssal faunas are fragmentary. There are very few
data on the distribution of species, while data on anatomy
are almost absent.

Several rare and undescribed species of Aforia have been
found recently by Soviet deep-sea expeditions. Our inves-
tigations of the morphology of their shells, radulae, and
soft parts have allowed us (1) to revise, to some extent, the
generic composition and to erect infrageneric taxa, (2) to
specify the identity and distribution of bathyal and abyssal
species (of which three species and one subspecies appear

to be new), and (3) to analyze the functional morphology
of the digestive system of the species studied.

For the comparative analysis of Aforra morphology, an
investigation was carried out of the anatomy of the genus
type species, A. circinata (Dall), which is not a true deep-
sea species.

All type specimens of described species are deposited in
the Zoological Museum of Moscow State University. Reg-
istration numbers are indicated in the descriptions of species.

MATERIALS anp METHODS

Materials for the study were collected by Soviet expeditions
on the research vessels Vityaz, Dmitry Mendeleev, Akademik
Kurchatov, and Gidrobiolog. Coordinates of stations where
mollusks were collected are listed in the descriptions of
species.

Page 106

The morphology of the digestive system was studied
histologically. The anterior part of the system (including
the proboscis with rhynchodaeum, poison gland, and a part
of the oesophagus) or the molluscan body after removing
the visceral mass and mantle were dehydrated and embed-
ded in paraffin; sections 8-10 um thick were cut. Sections
were stained with haematoxylin-eosin and Mallory’s stain.
Semidiagrammatic representations of the anterior part of
the digestive system were made. Poison and salivary glands,
together with the radular sac, were represented stereo-
scopically, but the nerve ring was not figured. In studies
of the odontophore of Aforia circinata, part of the buccal
mass with radular sac was sectioned transversally.

Examinations of the mantle complex of organs and the
penis were carried out with a stereomicroscope at mag-
nifications of 16-32 times. Radulae for light microscopy
were removed together with the radular sac and placed
into a sodium hypochlorite solution to dissolve the tissues,
with subsequent transfer to distilled water, cleaning, and
embedding in glycerol. Radular teeth of two species were
also prepared for scanning electron microscopy. After de-
hydration in alcohol and acetone, the teeth were mounted
on sticky tape, coated with gold, and examined with a
JSM-50A scanning electron microscope.

GENERAL ANATOMY oF
EXAMINED SPECIES

The body of deep-sea species of Aforia lacks pigmentation.
The head is well distinguished from the body; eyes are
absent. The morphology of the mantle complex is similar
in all species. The osphradium and gill are large, the
hypobranchial gland is moderately developed, and an anal
gland is absent. All species examined have an accessory
pedal gland situated in the depression in the middle part
of the marginal glandular cleft. The epithelial lining of
the accessory gland is similar to the rest of the marginal
cleft. The most probable function of the gland is lubrication
of the foot.

Close attention was paid to the anterior part of the
digestive system, as its morphology is the most variable
among Turridae. The generalized scheme of organs of the
body haemocoel of Aforia is represented in Figure 4A.

The species have a more or less long proboscis situated
in the rhynchocoel (rhynchodaeal cavity or proboscis
sheath). The proboscis can be stretched out through the
rhynchostome, which is surrounded with a very large,
powerful sphincter. The buccal mass lies at the base of
the proboscis. The buccal tube leads from the buccal cavity
to the mouth at the tip of the proboscis. The radular sac
opens into the buccal cavity. Near the entrance of the
radular sac two ducts of salivary glands open. Large sal-
ivary glands, which may unite to form a single large one,
are placed near or above a large nerve ring (not figured).
A long poison gland opens ventrally behind the buccal
mass. The poison gland has a large and powerful distal
muscular bulb that functions as a propulsive organ.

The Veliger, Vol. 30, No. 2

SYSTEMATIC DESCRIPTIONS
Class Gastropoda
Subclass Pectinibranchia Blainville, 1814
Order Toxoglossa Gray, 1853
Family Turridae Swainson, 1840
Subfamily Turriculinae Powell, 1942!
Genus Aforia Dall, 1889
Type species: Plewrotoma circinata Dall, 1873 (O.D.).

The mollusks under consideration have been described
in such genera as Pleurotoma, Leucosyrinx, Aforia, Ireno-
syrinx, or Sterraxis. However, in recent works only the
latter three names are used.

The genus Jrenosyrinx, with type species Pleurotoma
(Leucosyrinx ) goodei Dall, 1890, was described by DALL
(1908) for species close to those of Aforia but differing (at
least as type species) by the structure of the operculum.
In adult specimens of J. goode: the operculum has a sub-
central nucleus and looks like that of Buccinum whereas
the Aforia representatives have an elongate operculum with
a terminal nucleus. Subsequently, however, authors con-
sidered these differences insignificant (GRANT & GALE,
1931; POWELL, 1942, 1966, 1969; MCLEAN, 1971). We
agree with this subsequent opinion because the considered
group of species is rather homogenous and the species have
similar morphologies of the shell, radular teeth and soft
body, while the operculum with subcentral nucleus is known
only for A. goode:. Such opercular morphology of the spec-
imen studied by Dall can probably be considered an ab-
normal individual aberration caused by damage during
growth, which also occurs sometimes in other turrids. This
point of view is supported further by the fact that opercula
of younger specimens also investigated by DALL (1908)
have terminal nuclei similar to those of other species of
Aforia. The division of Aforia and Irenosyrinx proposed by
BOUCHET & WAREN (1980), based only on the fact that
the type species of Aforia is a shallow-water boreal north
Pacific species whereas that of [renosyrinx is an abyssal
eastern Pacific species, is considered groundless.

The monotypic genus Steiraxis was established by DALL

' POWELL (1969) and CERNOHORSKY (1972) considered that
the name Turriculinae Powell, 1942, cannot be used, being a
junior homonym and, therefore, the available name for this taxon
would be Cochlespirinae Powell, 1942. Recently, some authors
have accepted this statement. However, according to the Inter-
national Code of Zoological Nomenclature, the names Turriculinae
Carpenter, 1861, and Turriculinae A. Adams, 1846, based on
Turricula Fabricius, 1823 (Mitridae) (non Jurricula Schumacher,
1817 [Turridae]) are not senior homonyms of Turriculinae Pow-
ell, 1942 (Article 54[1]), since the former two names are invalid
(Article 39) and unavailable (Article 11[e]). Therefore, Turric-
ulinae Powell, 1942, should be considered as an available and
valid name.

A. V. Sysoev & Yu. I. Kantor, 1987

(1896), with type species Pleurotoma (Steiraxis) aulaca Dall,
1896. According to Dall and all later authors, the principal
feature separating this genus from Jrenosyrinx (=Aforia)
is stronger spiral sculpture equally developed on the whole
surface of the shell whorls. However, the presence of the
below-described abyssal species A. abyssalis sp. nov., which
has sculpture intermediate between typical Aforia and
Steiraxis, forces us to place S. aulaca in the genus Aforia
while the name Stezraxis can be used for a subgenus within
Aforia.

Peculiarities of the shell and radular tooth morphology
and bathymetric distribution of the species of Aforia allow
us to divide the genus into five subgenera. The diagnostic
features of the subgenera are summarized in Table 1.

Subgenus A/oria s.s.

The shell spiral sculpture is represented by narrow, low
ribs, being very slight on the shoulder. A weakly to mod-
erately pronounced spiral keel is usually situated on the
lower part of the shoulder. Marginal teeth of the radula
are very small, and the shell height-tooth length ratio
exceeds 100 (up to 180).

Species of the subgenus inhabit sublittoral and bathyal
waters of the Pacific, the southwestern Atlantic, and the
southeastern part of the Indian Ocean.

From our point of view the following nominal species
should be included in the nominal subgenus: Aforia circi-
nata (Dall, 1873), A. insignis (Jeffreys, 1883), A. magnifica
(Strebel, 1908), A. lepta (Watson, 1881), A. staminea (Wat-
son, 1881), A. gonioides (Watson, 1881), A. gooder (Dall,
1890), A. persimilis (Dall, 1890), A. persimilis leonis (Dall,
1908), A. persimilis blanca (Dall, 1919), A. amycus (Dall,
1919), A. kinkaidi (Dall, 1919), A. hondoana (Dall, 1925),
A. okhotskensis Bartsch, 1945, A. chosenensis Bartsch, 1945,
A. sakhalinensis Bartsch, 1945, A. diomedea Bartsch, 1945,
A. japonica Bartsch, 1945, and A. moskalevi Sysoev &
Kantor, sp. nov.

The above list includes names that have been only pro-
posed, but at present we cannot estimate the validity of
many of them because, on the one hand, we have too little
material and, on the other hand, a detailed study on the
shallow-water species systematics was beyond the scope of
our work. It should be noted that, according to many
authors, most if not all of the names proposed by BARTSCH
(1945) should be synonymized with A. circinata (see
POWELL, 1969) and all bathyal eastern Pacific species should
be considered as a single species, A. goode: (see MCLEAN,
1971).

Aforia (Aforia) circinata (Dall, 1873)
(Figures 3A, C-E, 4B, C, 7A—D)

Material: Our specimens were collected near Iturup Island
(Kurile Islands) at a depth of about 100 m (R/V Gidro-
biolog).

Page 107

Digestive system (Figure 7): The proboscis is long; in
studied specimens it was stretched out through the rhyn-
chostome. The buccal mass is large and pyriform, with a
deep fold at the upper part. The walls of the buccal mass
are thick, becoming thinner in the anterior part. The buccal
tube is of a small diameter without folds along the buccal
mass. The rhynchodaeum is strongly folded. The buccal
tube forms a small expansion with a sphincter near the
proboscis tip. The salivary glands are united as one large
gland located above the oesophagus. Paired salivary ducts
open into the radular sac near its entrance to the buccal
cavity. The epithelium of the buccal cavity forms high
folds, the largest of which are at the bottom of the cavity
near the entrance of the radular sac (Figure 7B). The
odontophore is of medium size with four subradular car-
tilages (Figure 7D) united in two pairs and connected by
a muscular symphysis in the anterior part of the odonto-
phore (Figure 7C). The radular sac is surrounded with a
thick layer of muscles and is lined inside with a thick
cuticular layer. The poison gland is large, with a greatly
decreased diameter near its opening into the oesophagus.
The muscular bulb is of medium size and oval. The oesoph-
agus sharply increases in diameter posterior to the nerve
ring. The stomach typically has a U-shape form and re-
ceives two ducts of the digestive gland. The radula is of
typical form for the genus (Figures 3C-E). The central
teeth are weak and thin. The marginal teeth are small.
The shell height-tooth length ratio is 180.0.

Aforia (Aforia) lepta (Watson, 1881)
(Figures 1F, G, 5B, 6E-H, 8A-E)

Pleurotoma (Surcula) lepta WATSON, 1881:391, 1886:288, pl.
XVIII, fig. 7.

Material: R/V Dmitry Mendeleev, station 1276, 48°25’S,
171°42’E (SE of New Zealand), depth 1100-1200 m, trawl
Sigsbee, 1 specimen.

Shell: The shell of our specimen is very similar to that
described by Watson (1886), differing in its smaller size
(the shell height is 14.1 mm), less numerous whorls, and
less well-developed spiral keel, especially on the penulti-
mate whorl; spiral sculpture is more uniform, and inter-
calate threads between primary ones are absent.

The protoconch sculpture and also the operculum, rad-
ula and soft-body morphology, which were not studied
previously, are described here. The operculum is small
and drop-shaped (Figure 5B). The protoconch consists of
1.5 rapidly increasing whorls sculptured with very weak,
thin, and inconspicuous spiral folds.

Anatomy (Figures 6E-H): The mantle is thin and the
osphradium and gill are clearly seen through it. The siphon
is short and contracts strongly during fixation. The pro-
podium of the foot is narrow with a deep cleft; the accessory
pedal gland is weak. The head is well distinguished from
the body; the tentacles are short and rounded at the tip.

Page 108

Table 1

Characters of the subgenera of Aforza.

Shell
height-
tooth
Sub- Spiral length
genus Spiral ribs keel ratio
Aforia s.s. narrow, low, very present, 107-180
slight on the shoul- var-
der iously
devel-
oped
Stevraxis very strong, equally de- present, about 70
veloped throughout strong
the shell surface
Abyssa- narrow, prominent, none 57-90
foria equally developed
throughout the shell
surface
Dallaforia strongly inequal on the _— none about 100
shoulder and on the
rest of the whorl
Palaeo- narrow, weak, present, —
aforia smoothed on the double

shoulder

The rhynchostome has well-developed lips; its sphincter
is very large.

Mantle complex (Figure 6G): The osphradium and gill
are very large. The gill lamellae are tall and triangular;
their height is nearly equal to the base width. At the inner
side of the lamella a thickened cuticulized flagellum is
situated. The flagellum adheres to the lamella. The gill
extends nearly to the mantle outer edge but its lamellae
are low there. The osphradium is flattened. The hypo-
branchial gland is poorly developed and is covered with a
thick gel-like mucosal layer. The pallial oviduct is of small
diameter and the female gonopore opens on a small round-
ed eminence. The rectum has a very small diameter. It lies
along the surface of the oviduct; the anus opens nearer to
the outer edge of the mantle than the gonopore does. There
is a short and narrow transverse fold in the right part of
the mantle.

Digestive system (Figure 8): The proboscis is small; its
epithelium is formed by very tall gobletlike cells (Figure
8B). The buccal mass is of medium size with relatively
thin walls. The buccal tube forms a fold along the buccal
mass. In the anterior part, the buccal tube forms a small
sphincter. Retractor muscles of the proboscis pass along
its lumen and attach near the tip. The rhynchodaeum is
folded and covered with a thick cuticular layer. The paired
salivary glands are large, and their ducts are of small
diameter, slightly coiling. The muscular bulb of the poison
gland is small. Odontophore cartilages are absent, being
replaced by a strong muscular fold. The oesophagus grad-

The Veliger, Vol. 30, No. 2

ually widens posterior to the entrance of the poison gland.
The stomach is typically U-shaped, containing two ducts
of the digestive gland. The central radular teeth are very
thin (Figure 8D). The marginal teeth are small (Figures
8D, E). The shell height-tooth length ratio is 100.7.

Distribution: The species was previously known from
two localities—the Australian-Antarctic Rise (R/V Chal-
lenger, station 157, 53°55'S, 108°35’E, type locality) and
near Kerguelen Island (WATSON, 1886; CANTERA &
ARNAUD, 1984). Our specimen was found in the New
Zealand underwater plateau and, therefore, the species
range is greatly extended eastward. The species lives at
depths of 360 to 3560 m.

Aforia (Aforia) moskalevi
Sysoev & Kantor, sp. nov.

(Figures 1E, H, 5A, 6A—D, 9A-G)

Material: R/V Dmitry Mendeleev, station 1314, 59°58’S,
158°07'E (SW Pacific), depth 3010-3030 m, trawl Sigsbee,
2 specimens—holotype (No. LC 5360) and paratype (No.
LC 5361).

Description of holotype: The fusiform shell is thin and
consists of 4.5 preserved whorls. The protoconch is lost,
as the first preserved whorl is eroded. Whorls are slightly
convex and angulate at the periphery. The whorl shoulder
is flattened and sloping. There is a very weak spiral fold
on the shoulder of the body whorl. Axial sculpture is
represented only by numerous thin growth lines, some of
them being rather more pronounced, especially below the
shoulder. Spiral sculpture of the upper part of the whorl
consists of threadlike, weak, flattened ribs irregularly dis-
placed and separated by interspaces twice as wide. On the
lower part of the whorl, spiral ribs are larger, narrow,
rounded, irregularly disposed, and separated by inter-
spaces that are 2—4 times wider than rib widths. In some
interspaces, there are much weaker secondary ribs. As the
spiral ribs cross the strongest growth lines, they form re-
ticulate sculpture. The aperture is wide and oval. The
outer lip is broken. The inner lip is smoothly curved, coated
with thin callus. The siphonal canal is long, slightly curved.
The sinus, judging by growth lines, is deep, wide, and
rounded; its apex is situated some distance above the middle
of the whorl shoulder. The shell color is gray. The shell
height is 33.4 mm, the height of the body whorl is 25.5
mm, the aperture height is 20.8 mm, and the shell diameter
is 12.2 mm.

The paratype is smaller (the shell height is 27.2 mm)
and poorly preserved. Its shell is quite similar to the ho-
lotype. We have studied the anatomy of the paratype.

The operculum is small and roundly triangular, with a
terminal nucleus (Figure 5A).

Anatomy (Figures 6A-D): The mantle is thick, and the
osphradium and gill are seldom seen through it. The man-
tle edge is uneven; it has a distinct notch corresponding to

E G

Figure 1

A and B, Aforia crebristriata (Dall), R/V Vityaz, stat. 4173, shell height of 40.4 mm. C and D, A. kuprtyanovi sp.
nov., holotype. E and H, A. moskalevi sp. nov., holotype. F and G, A. lepta (Watson), R/V Dmitry Mendeleev,
stat. 1276, shell height of 14.1 mm.

Figure 2

A-G, Aforia abyssalis sp. nov. A and B, holotype. C, paratype, R/V Vityaz, stat. 5624, shell height of 31.8 mm.
D, paratype, R/V Vityaz, stat. 5624, shell height of 31.0 mm. E, paratype, R/V Vityaz, stat. 3594, shell height of

39.0 mm. F, paratype, R/V Vityaz, stat. 4104, shell height of 16.8 mm. G, paratype, shell sculpture. Scale bar =
1 mm.

A. V. Sysoev & Yu. I. Kantor, 1987 Page 111

Figure 3

A, Aforia circinata (Dall), shell height of 52.4 mm. B, A. aulaca alaskana subsp. nov., holotype. C-E, SEM photographs
of radula of A. circinata.

Page 112

The Veliger, Vol. 30, No. 2

Figure 4

A, general diagrammatic section of the anterior part of Aforia digestive sytem. B-D, marginal teeth of Aforza (B, A.
circinata. C, the same, transverse section. D, A. abyssalis). Key to abbreviations for all figures: AG, accessory pedal
gland; AO, anal opening; BT, buccal tube; BM, buccal mass; BW, body wall; CT, central tooth; DG, digestive
gland; FT, fold of buccal tube; FG, female gonopore; G, gill; H, head; HG, hypobranchial gland; LM, longitudinal
muscles; LR, lip of rhynchostome; MB, muscular bulb; MG, male gonopore; MT, marginal tooth; N, nephridium;
OC, odontophoral cartilage; OE, oesophagus; OP, operculum; OS, osphradium; PG, poison gland; PO, pallial
oviduct; PR, proboscis; PRM, retractor muscles of the proboscis; PP, propodium; PS, proboscidal sphincter; RA,
radula; R, rectum; RD, rhynchodaeum; RS, rhynchostome; RT, radular tooth; S, siphon; SD, salivary duct; SG,
salivary gland; SP, sublingual pouch; SR, rhynchostomal sphincter; ST, stomach; T, tentacles; TM, transverse

muscles.

the anal sinus of the shell. The head is well distinguished
from the body. The tentacles are long and flattened. The
propodium is very narrow, and the accessory pedal gland
is poorly developed. A large rhynchostomal sphincter is
present.

Mantle complex (Figure 6C): The gill and osphradium
are large, the latter being 7 of the gill length. Gill lamellae
are tall and triangular. The thickened flagellum of the gill
is free in its upper part to form a rounded growth. The
hypobranchial gland is well developed, and forms about
30 closely placed folds. A long siphon with a large dis-
tributive valve at its base is. well developed. The rectum
is of small diameter with a small but distinct anal papilla.

Digestive system (Figure 9): The proboscis is long, nar-
rowing towards its tip. Powerful proboscis retractor mus-
cles are attached mostly to the integument of the body sinus
roof. The buccal mass is not large. The buccal tube is
surrounded with a relatively thin layer of circular mus-

culature to form a long double fold along the buccal mass.
There is a small sphincter of the buccal tube at its tip in
which a radular marginal tooth was found to be held
(Figure 9B). The muscular bulb of the poison gland is
rather small and oval. The salivary glands join to form a
single gland placed above the oesophagus and embracing
it. The salivary ducts are relatively thick and twist slightly.
The odontophore is small (Figure 9C); there are four
subradular cartilages forming pairs on each side. The paired
cartilages fuse in the anterior part of the odontophore and
the fused pairs are connected with a muscular symphysis.
The radular sac is lined with a thick layer of cuticle. The
rachidian tooth of the radula is thin, weak, and curved,
with a smooth anterior edge. The marginal teeth (Figures
9D, E) are short, broad, and their distal parts are optically
more dense than the basal parts. The length of a marginal
tooth is 0.24 mm. The shell height - tooth length ratio is
113.3. The oesophagus abruptly widens behind the en-
trance of the poison gland. The stomach is of the typical

A. V. Sysoev & Yu. I. Kantor, 1987

U-shape, with two ducts of the digestive gland. The spec-
imen dissected is an immature female.

Remarks: This species is closest to Aforia kupriyanovi sp.
nov., differing by the weak development of spiral ribs on
the body-whorl shoulder, the lesser number of ribs, the
flattened whorl shoulder, and the much smaller marginal
teeth (as measured in relative values).

Distribution: The species was found in the abyssal zone
of the region southward from the Hyort trench (south-
western Pacific).

Subgenus Steiraxis Dall, 1896
Type species: Pleurotoma (Steiraxis) aulaca Dall, 1896 (O.D.).

Spiral sculpture consists of very strong, prominent, near-
ly rectangular in section ribs equally developed throughout
the shell surface. The spiral keel is strong and situated at
the whorl periphery. Marginal teeth of the radula are very
large, and the shell height-tooth length ratio is about 70.

The subgenus includes a single species with two sub-
species (Aforia aulaca aulaca (Dall) and A. aulaca alaskana
subsp. nov.) living at abyssal depths of the eastern Pacific
along the coast of North and Central America.

Aforia (Steiraxis) aulaca alaskana
Sysoev & Kantor, subsp. nov.

(Figures 3B, 5D, 12F-H)

Material: R/V Vityaz, station 6109, 56°17.7'N, 139°43.3’W
(Gulf of Alaska), depth 3460 m, Sigsbee trawl, 1 specimen
(holotype, No. LC 5362).

Description of holotype: The shell is small, fusiform, and
consists of 5 whorls. The upper whorls are significantly
eroded. The whorls are slightly convex, angled at the pe-
riphery where a spiral keel is placed. The whorls are
divided by very shallow, poorly visible sutures. The whorl
shoulder is flattened. Axial sculpture is represented only
by very thin, numerous growth lines. Spiral sculpture con-
sists of the keel situated at the whorl periphery and also
of strong, prominent, nearly rectangular in section ribs
covering all the shell surface. The width of ribs varies
insignificantly. Sometimes, there is an additional thin rib
in the interspace between the more prominent ribs. There
are two ribs on the spiral keel. The ribs are much lower
on the shell base and on the anterior canal. Interspaces
between ribs vary in their width, being in most cases equal
to the ribs themselves or slightly wider. There are 15 spiral
ribs on the penultimate whorl and 48 on the body whorl;
11 of the latter are disposed between the keel and the
suture. The ovate aperture gradually transforms into the
long siphonal canal, which is slightly curved and widens
toward the end. The inner lip is coated with a wide but
thin callus. The anal sinus, judging by growth lines, is
wide, rounded, and not very deep, its apex being placed
approximately in the middle of the space between the

Page 113

Figure 5

Opercula of Aforia species. A, A. moskalevi, paratype. B, A. lepta.
C, A. crebristriata. D, A. aulaca alaskana, holotype. E-G, A. abys-
salis (E, paratype, R/V Vityaz, stat. 5624. F, paratype, R/V
Vityaz, stat. 3594. G, paratype, R/V Vityaz, stat. 2074). H, A.
kupriyanovi, holotype. Scale bar = 1 mm.

suture and the keel. The shell color is light brown. The
shell height is 25.8, the body-whorl height is 20.0, the
height of the aperture is 16.5, and the shell diameter is 11
mm.

Anatomy: The rhynchostomal sphincter is very poorly
developed, compared to other species. The rhynchostome
has weak, small rhynchostomal lips. A small accessory
propodial gland is placed on the bottom of the propodial
cleft.

Mantle complex of organs: The mantle morphology is
typical for the genus. The mantle edge is serrated. The
ctenidial lamellae are high, and there is a thick cuticular
basal flagellum at the inner edge. The hypobranchial gland
is poorly developed.

Digestive system: The proboscis (Figure 12F) is typical
for the genus. The buccal mass is small, and the buccal
tube is surrounded by a rather thick layer of circular
musculature. Near the tip of the proboscis the buccal tube
forms a sphincter (Figure 12G). Powerful and large pro-
boscis retractors are attached to the expansion of the buccal
tube at some distance from the proboscis tip. It is possible
that the end of the buccal tube can be everted. The poison
gland is thick and has a very large muscular bulb. The
central radular tooth is large; it has one cusp on its frontal
edge and long, narrow, curved blades (Figure 12H). The
marginal teeth are long and slightly curved (Figure 12H)
(0.38 mm length). The shell height-tooth length ratio is
67.9.

Remarks and distribution: Aforia aulaca alaskana subsp.
nov. differs from the nominal subspecies in having a small-
er shell (the height of holotype shell of A. aulaca aulaca is
60 mm) that is covered with spiral ribs that are not sharp

The Veliger, Vol. 30, No. 2

Page 114

A. V. Sysoev & Yu. I. Kantor, 1987

oy
QI ,

6,
re

Page 115

Ss
EOP OTS

30.

Figure 7

Morphology of digestive system of Aforza circinata, shell height of 49.0 mm. A, semidiagrammatic section of anterior
part of digestive system. B, transverse section across the radular sac at the anterior part of odontophore. C, the
same, medial part of odontophore. D, the same, basal part of odontophore. See Figure 4 for key to abbreviations.

but rectangular in side view, and with interspaces between
them being equal or slightly wider than the rib width (z.e.,
the interspaces between ribs are wider than in the nominal
subspecies). The most striking difference between the sub-
species is the shape of the radular teeth. The drawing of
the radula of the holotype specimen of A. aulaca aulaca
(according to the catalogue number) was published by
POWELL (1966:text fig. 26). The marginal teeth of the new
subspecies are wider; the central tooth is large and cres-
centlike with a cusp on its frontal edge whereas the central
tooth of the nominal subspecies is represented by a narrow
small plate that is protracted along the subradular mem-
brane and bipolarly sharply terminating. Moreover, the
two subspecies differ in their geographic distribution. Afor-

ia aulaca aulaca is found along the Pacific coast of North
and Central America from northern California to the Gulf
of Panama (DALL, 1908; PARKER, 1964; Rokop, 1972).
Aforia aulaca alaskana has been recorded so far only in the
Gulf of Alaska. It is interesting to note that both subspecies
have a similar vertical range, 3241-3798 and 3460 m
respectively.

Subgenus Dallaforia
Sysoev & Kantor, subgen. nov.
Type species: [renosyrinx ? crebristriata Dall, 1908.

Spiral sculpture is represented by very strong, wide,
prominent ribs situated below the whorl shoulder and

Figure 6

Soft body of Aforia species. A~D, A. moskalevi, paratype (A and B, whole body. C, mantle complex. D, single
lamella of the gill). E-H, A. lepta (E and F, whole body. G, mantle complex. H, distal part of female pallial
gonoduct and rectum). I-L, A. crebristriata (I and J, whole body. K, mantle complex. L, penis). M-P, A. abyssalis,
paratype, shell height of 39.0 mm (M and N, whole body. O, mantle complex. P, penis). Scale bar = 2 mm. See

Figure 4 for key to abbreviations.

Page 116

Ses
LN

tA LRA snr - AL RA

a eS Q
3 AAI) A Qn
ve Soo” Las Lala Sas

o-Smm

The Veliger, Vol. 30, No. 2

Z
anh

A>

R
&>
ee SS

Figure 8

Morphology of digestive system of Aforia lepta. A, semidiagrammatic section of anterior part of body (the foot is
hatched). B, magnified tip of the proboscis. C, magnified part of body wall. D and E, radula. Scale bar for B and

C = 0.1 mm. See Figure 4 for key to abbreviations.

weak, flattened ribs on the shoulder. A spiral keel is absent.
Marginal teeth of the radula are of middle size, and the
shell height-tooth length ratio about 100.

The subgenus is represented only by the type species
living in abyssal regions of the northeastern Pacific.

Aforia (Dallaforia) crebristriata (Dall, 1908)
(Figures 1A, B, 5C, 6I-L, 10A-C)
TIrenosyrinx ? crebristriata DALL, 1908:272, pl. 13, fig. 10.

Material: R/V Vityaz, station 4173, 44°54'N, 128°32’W
(off Oregon), depth 2830-2840 m, trawl Sigsbee, 3 spec-
imens.

A detailed description of the shell of Aforia crebristriata
was given in the original description of the species. There-
fore, we add data only on the operculum, anatomy and
radula, which are absent in Dall’s article.

Operculum: The operculum is small in comparison with
other species of the genus; its shape is nearly triangular,
with a terminal nucleus. The part most remote from the
nucleus of the operculum of one of our specimens has a
rounded projection (Figure 5C) that appears the probable
result of a disturbance during its growth.

Anatomy (Figures 6I-L): The studied specimen has a
shell height of 30.0 mm. The tentacles are long and cy-
lindrical. The propodium is very narrow; the marginal
cleft is shallow. The accessory pedal gland is poorly de-
veloped. At both sides of the propodium base, the meta-
podium forms rather long and large palps. The mantle is
thin and the osphradium and gill are clearly seen through
it. The mantle edge is scalloped; its projections correspond
to spiral ribs. The mantle does not cover the head base.

Mantle complex (Figure 6K): The osphradium and the
gill are large. The narrow gill is formed by tall triangular
lamellae. The basal flagellum is weakly thickened and
attached to the lamella along nearly its entire length. The
gill axis is very thin. The osphradium is greenish. The
hypodermal gland is covered with a thick layer of gel-like
mucosa. The siphon is long and has a small distributive
valve at its base. The rectum is of small diameter; there
is a small palp formed by the rectal wall.

Digestive system (Figure 10): The proboscis is long. The
buccal mass has rather thin walls. The buccal tube is
surrounded by a moderately thick layer of circular muscles;
it forms a long fold along the buccal mass. Salivary glands
unite as one gland located above the oesophagus. The

A. V. Sysoev & Yu. I. Kantor, 1987

Page 117

Figure 9

Morphology of digestive system of Aforia moskalevi, paratype. A, semidiagrammatic section of the anterior part of
digestive system. B, magnified tip of the proboscis. C, longitudinal section across the anterior part of radular sac.
D, radula in natural position. E-G, marginal tooth, various projections. Scale bar for B and C = 0.2 mm. See

Figure 4 for key to abbreviations.

salivary ducts are paired and of small diameter. Two odon-
tophoral cartilages are very large; they unite in the anterior
part of the odontophore (Figure 10B). The epithelium of
the radular sac and the buccal cavity is lined with a thin
cuticular layer. The large proboscis retractor muscles are
placed near the proboscis walls and attach to the proboscis
wall near its tip. The muscular bulb of the poison gland
is large. The oesophagus abruptly widens behind the nerve
ring. The poison gland opens into the oesophagus rather
far from the radular sac. The radular sac is surrounded
by a thick muscular layer. The central radular tooth has
moderately wide, nearly straight, and almost rectangular
blades, and one thin and long cusp on the frontal edge.
The marginal teeth are wide, short, slightly curved, and
very small (their length is 0.29 mm when the shell height
is 30.2 mm). The shell height-tooth length ratio is 104.1.
The stomach is of the typical U-shape, and contains paired
closed ducts of the digestive gland.

Reproductive system: The vesicula seminalis is very large,
formed by numerous very small loops of the seminal duct.
The penis is relatively short and broad (Figure 6L), with
slightly folded walls. The genital papilla is large, rounded,
and surrounded by a circular fold. The male gonopore
opens somewhat laterally in a small invagination.

Distribution: The species inhabits the upper abyssal zone
along the northwestern coast of North America from the
Gulf of Alaska to Oregon at depths of 2830 to 2869 m.
Type locality—station 2859 of R/S Albatross (off Sitka,
Alaska).

Subgenus Abyssaforia
Sysoev & Kantor, subgen. nov.

Type species: Aforia (Abyssaforia) abyssalis Sysoev & Kan-
tor, sp. nov.

Spiral sculpture is represented by numerous narrow,
prominent ribs equally developed throughout the shell sur-
face. A spiral keel is absent or a trace is retained as a slight
angulosity of the whorl shoulder visible on early whorls.
Marginal teeth of the radula are large, and the shell height-
tooth length ratio is less than 100 (57-90).

Representatives of the subgenus live in abyssal regions
of the Pacific and the northern Atlantic.

The subgenus includes three species—A. abyssalis Sy-
soev & Kantor, sp. nov., A. hypomela Dall, 1889, and A.
kupriyanovi Sysoev & Kantor, sp. nov.

Most deep-water species of Aforia s.s. possess spiral
sculpture close to that of Abyssaforia.

Page 118

The Veliger, Vol. 30, No. 2

Figure 10

Morphology of digestive system of Aforia crebristriata. A, semidiagrammatic section of the anterior part of digestive
system, B, longitudinal section across the anterior part of radular sac. C, radula. See Figure 4 for key to abbreviations.

Aforia (Abyssaforia) abyssalis
Sysoev & Kantor, sp. nov.

(Figures 2A-G, 4D, 5E-G, 6M-P, 11A-F)

Material: R/V Vityaz, station 2074, 42°32’N, 150°41’E
(SE of Iturup, Kurile Islands), depth 5140 m, trawl Sigs-
bee, 2 specimens; station 2119, 46°07.8’N, 155°16’E (E of
Urup, Kurile Islands), depth 5070-5090 m, trawl Sigsbee,
1 specimen (holotype, No. LC 5363); station 3594,
40°55.2’N, 144°53.3’E (SE of Hokkaido, Japan), depth
3880-3900 m, trawl Sigsbee, 1 specimen and 1 shell; sta-
tion 4104, 41°07.5'N, 159°53.9'W (NE Pacific), depth
5430-5456 m, trawl Sigsbee, 1 juvenile specimen; station
5624, 45°26'N, 154°12’E (E of Urup, Kurile Islands),
depth 5220 m, trawl Galathea, 22 specimens (mostly ju-
veniles) and 1 shell. All the paratypes are stored as No.
LC 5364.

Description of holotype: The shell is medium in size for
the genus, elongately fusiform, thin, and consists of 5 pre-
served whorls. The protoconch and upper whorls are se-
riously eroded. Whorls are weakly convex, somewhat an-
gled at the periphery; the whorl shoulder is flattened. Axial
sculpture is represented by growth lines that are numerous,
clear, and very thin; some of them, probably reflecting

significant interruptions of shell growth, clearly differ from
others in their prominence. There are 6 of these growth
lines on the body whorl. Spiral sculpture consists of thin,
clear, pronounced, cordlike ribs separated by always larger
interspaces. The ribs are separated from each other by
uneven intervals; they are closest at the periphery of the
whorl where the interspaces are 1.5-2 times wider than
the width of the rib itself. They are most distant from each
other on the whorl shoulder where interspaces are 3-7
times wider than those of the ribs. On the body whorl, 1
or 2 weak, thin accessory ribs may be situated in the
interspaces. There are 15 spiral ribs on the penultimate
whorl and about 60 on the body whorl, including the canal.
The aperture is narrow and ovate; its outer lip is thin.
The inner lip is gradually curved, covered by translucent
callus, and develops a small projection when passing into
the canal. The canal is long and curved. The shell color
is grayish cream. The height of the shell is 56.3 mm, the
height of the body whorl is 43.0 mm, the height of the
aperture is 35.1 mm, and the shell diameter is 21.0 mm.

Younger paratype specimens are characterized by more
convex and angled shell whorls. A tendency can be noted
in some young specimens to develop a slight fold at the
upper part of the whorl near the suture. The spiral ribs

A. V. Sysoev & Yu. I. Kantor, 1987

) SN
f SS y} * an mT mt <Q PG
G7 MRT WWW SW Se
, atte 9 SG
= Dy RAIS ) S
/ att 7 \ ; ja
Gal cc 2 Res

ERE

Page 119

A
VA
NS
wy UR\_@
RMA

2 Ss
Gress

Figure 11

Morphology of digestive system of Aforia abyssalis, paratype, shell height of 39.0 mm. A, head. B, semidiagrammatic
section of the anterior part of digestive system. C, magnified tip of the proboscis. D, radula of paratype (R/V
Vityaz, stat. 3594, shell height of 39.0 mm). E, the same (R/V Vityaz, stat. 5624, shell height of 25.7 mm). F,
marginal tooth of paratype (R/V Vityaz, stat. 2074, shell height of 74.2 mm). Scale bar for D-F = 0.1 mm. See

Figure 4 for key to abbreviations.

in paratypes, especially in young ones, sometimes are more
flattened, wider, and closer to each other, especially on the
whorl shoulder. The growth lines of smaller shells, par-
ticularly on upper whorls, may be more rough, prominent,
and can form some kind of weak axial folds on the shell
surface. The shell height of the largest paratype is 74.2
mm.

The operculum is ovate and large (Figures 5E-G).

Anatomy (Figures 6M-P): (The anatomy of a paratype
from station 3594, having a shell height 39.0 mm, is shown
in the most Figures except 6P). The propodium is narrow,
and the marginal cleft is not deep. The accessory pedal
gland is situated almost at the central part of the cleft. The
mantle completely covers the head, which is well distin-
guished from the body. Tentacles are cone-shaped and
rounded at the tip. The rhynchostomal lips form a funnel.
The rhynchostome is small; its large and powerful sphinc-
ter constitutes the major part of the head volume.

Mantle complex (Figure 6O): The gill is very large; its
length is nearly equal to the mantle length. The lamellae

are tall and triangular, with poorly thickened lamellae at
their inner sides which completely adhere to the lamellae.
The osphradium is of medium size, and greenish. The
hypobranchial gland forms inconspicuous folds covered
with a thick layer of gel-like mucus. The rectum is of small
diameter, and its wall forms a small palp near the anus.

Digestive system (Figure 11): The proboscis is rather
short. The buccal mass is large and has thick walls. The
buccal tube forms a small fold along the buccal mass, The
salivary gland is paired; the right salivary gland is elongate
and the left one is more ovate. The salivary ducts are
slightly coiled, moderately thick, and open into the radular
sac near its entrance into the buccal cavity. The odon-
tophoral cartilages are very thin, narrow, and connected
in the anterior part by a transverse muscle. There are 4
cartilages, which are united in 2 pairs. The muscular bulb
of the poison gland is very large with a small lumen. The
oesophagus gradually widens behind the opening of the
poison gland. The stomach is of the typical U-shape and
contains a single duct of the digestive gland. The radular

Page 120

The Veliger, Vol. 30, No. 2

Figure 12

A-E) Aforia kupriyanovi, holotype. A, semidiagrammatic section of the proboscis. B, magnified tip of the proboscis.
C, head and the anterior part of the foot. D, radula. E, marginal tooth in lateral projection. Scale bar for D and
E = 0.1 mm. F-H, A. aulaca alaskana, holotype. F, semidiagrammatic section of the proboscis. G, magnified tip
of the proboscis. H, radula. Scale bar = 0.1 mm. See Figure 4 for key to abbreviations.

teeth show variability based on age. The younger specimen
has more short and broad marginal teeth (Figure 11E)
than the older one (Figure 11F). The central tooth has
one cusp which becomes sharper and longer during growth
of the mollusk. The length of the marginal tooth of the
specimen with the shell height of 25.7 mm is 0.30 mm,
with the shell height of 39.0 mm it is 0.44 mm, and with
the shell height of 74.2 mm it is 0.80 mm. The shell height-
tooth length ratios are 82.9, 88.6, and 90.5 respectively.

Reproductive system: One of studied paratypes (station
3594) is an immature female. The paratype from station
5624 is a mature male. Its vesicula seminalis is very large,
with numerous small loops of seminal duct. The penis
(Figure 6P) is long, flattened, and sharp at the frontal
edge. The male gonopore opens on a small papilla sur-
rounded with a circular fold.

Remarks: The species is conchologically very close to Afor-
1a hypomela Dall, differing in that the new species has
more numerous and narrow spiral ribs, a more curved
siphonal canal, different form and size of the radular teeth
(for A. hypomela see BOUCHET & WAREN, 1980:fig. 7),
and a different geographical distribution: A. hypomela is

an Atlantic species while A. abyssalis sp. nov. is presently
reported only from the Pacific.

Distribution: The species inhabits the lower abyssal zone
of the northern Pacific at depths of 3880 to 5456 m; most
records are from the northwestern Pacific.

Aforia (Abyssaforia) kupriyanovi
Sysoev & Kantor, sp. nov.

(Figures 1C, D, 5H, 12A—E)

Material: R/V Akademik Kurchatov, station 240, 23°47'S,
71°03'W, (off Antofagasta, Chile), depth 4300 m, trawl
Galathea, 1 specimen (holotype, No. LC 5365).

Description of holotype: The shell is of moderate size,
fusiform, thin, fragile, and consists of 5.5 preserved whorls.
A part of the protoconch is lost; the upper whorls are
seriously eroded. The shell whorls are convex, rounded,
and separated from each other by definite shallow sutures.
The body whorl occupies about % of the shell height.
Growth lines are weak and poorly visible. The spiral sculp-
ture consists of similar, low, cordlike, slightly wavy ribs
covering all the shell surface and separated from each other

A. V. Sysoev & Yu. I. Kantor, 1987

by interspaces that are 2-4 times wider than the ribs. The
ribs are placed more closely to each other at the whorl
periphery and more distant at the shell base. Two ribs of
the periphery of the body whorl are situated on a weak
eminence and look like a very poorly developed spiral keel.
There are 15 ribs on the penultimate whorl and 44 on the
body whorl including the canal. The aperture is wide and
ovate. There is a large, low knob at the upper portion of
the inner lip. The canal is long and curved. The anal sinus,
judging by growth lines, is wide, deep, and rounded. The
shell color is grayish white. The shell height is 26.4 mm,
the body-whorl height is 19.9 mm, the aperture height is
16.2 mm, and the shell diameter is 11 mm.

The operculum is ovate; its growth axis is strongly curved.

Anatomy: The propodium is narrow, the marginal cleft
is not deep, and the accessory pedal gland is situated at its
middle part. Diameter of the pedal gland is about 0.25
mm. The metapodium forms small palps at both sides of
the propodial base (Figure 12C). The head is elongate and
well distinguished from the body. The tentacles are long
and cylindrical. The rhynchostome is wide; its sphincter
is large.

The mantle complex is typical for the genus. The os-
phradium and the gill are large, and the mantle edge forms
a deep notch, corresponding to the anal sinus of the shell.
The distributive valve of the siphon is small. The gill
lamellae are tall, with a thickly cuticulized flagellum.

Digestive system: The proboscis is not large (Figure 12A).
The buccal mass is very large; its length exceeds 2 of the
proboscis length. The buccal tube forms a very long fold
along the mass. The buccal tube is surrounded by a rather
thick layer of circular muscles. At the tip of proboscis, the
buccal tube forms a small enlargement in which a single
radular marginal tooth was found to be held (Figure 12B).
The tooth basal part is held by the sphincter that is situated
at the base of the enlargement. Another sphincter is at the
tip of the proboscis. The retractor muscles of the proboscis
are rather small; they follow along the proboscis walls.
The buccal tube is connected with the proboscis walls by
numerous muscles. The central radular tooth has long
curved blades and one broad cusp on the frontal edge. The
marginal teeth are curved (Figures 12D, E), rather broad,
and small (0.46 mm). The shell height-tooth length ratio
is 57.4. The muscular bulb of the poison gland is large,
and elongate-oval. The stomach is of the typical U-shape,
containing two ducts of the digestive gland.

Remarks: The species is most similar to the abyssal species
Aforia hypomela Dall and A. abyssalis sp. nov., but differs
clearly by having a small shell, with rounded, strongly
convex whorls, stronger spiral ribs, and a long, consider-
ably curved siphonal canal, and different radular tooth
(especially the central one) form.

Distribution: The species lives in the abyssal zone of the
Peru-Chilean trench.

Page 121

Subgenus Palaeoaforia
Sysoev & Kantor, subgen. nov.

Type species: Aforza campbelli Durham, 1944.

Spiral sculpture consists of slight, narrow ribs that are
smoothed on the whorl shoulder and of two strong spiral
keels on the lower part of the whorl shoulder and on the
shell base.

The subgenus is represented mostly by fossil species
(Aforia campbell: Durham, 1944, A. ward: (Tegland, 1933),
A. addicotti Javidpour, 1973, A. clallamensis (Weaver, 1916),
A. tricarinata Addicott, 1966) reported from Oligocene and
lower Miocene deposits of western North America (JaA-
VIDPOUR, 1973). Aforia trilix (Watson, 1886) is the only
Recent species that can be probably included in this sub-
genus. Nevertheless the species’ taxonomic position (in-
cluding its belonging to Aforia) at present is uncertain and
needs further investigations.

An opinion on the possibility of isolating Oligocene A/or-
1a as a separate subgenus was earlier expressed by HICK-
MAN (1976) based on the presence of the second keel on
Oligocene shells.

DISCUSSION
General Morphology of Species of Aforia

Generally the organ morphology of studied systems is
very similar among subgenera and species of Aforza. We
could not find any significant differences at the subgeneric
level. The digestive system manifests probably the most
marked differences between species.

The rhynchodaeum, the wall of the proboscis sheath, is
folded in all species; its epithelium is represented by tall
secretory cells. In most species, the rhynchodaeum adheres
to the wall of the body haemocoel whereas in Aforia lepta
it is free all along its length to be connected only in places
to the haemocoel wall with thin muscles. An invaginable
part of the rhynchodaeum, such as is present in gastropods
with a pleurembolic proboscis, is absent in Aforia. How-
ever, most Aforia species can stretch the proboscis out of
the rhynchostome. This process is facilitated by secretions
produced by the secretory epithelial cells lining the pro-
boscis and the rhynchodaeum. Aforia lepta probably is an
exception. The proboscis epithelium of this species is formed
by very tall, thin, gobletlike cells (Figure 8B). It is difficult
to imagine that such cells would remain undamaged during
proboscis stretching and functioning in the environment.
The relative small size of the proboscis, as compared to
the proboscis sheath, seems also to be evidence that exten-
sion of this species’ proboscis is limited only to the rhyn-
chocoel. In all Aforza species, the proboscis retractor mus-
cles are represented by several moderately thick muscle
bands situated at the cavity perimeter along the proboscis
lumen. The most powerful muscles are attached to the
inner side of the body haemocoel wall. The retractors pass
near the proboscis walls to join often with the inner (lon-

Page 122

Table 2

Dependence of relative length of marginal teeth of Aforia
radulae on depth of species habituation.

Depths of
habituation of Shell
studied height—
specimens tooth length
Groups of species (meters) ratio
A. circinata, A. kinkaidi 100-240 150-180
A. lepta, A. moskalevi,
A. crebristriata 1200-3030 100-113

A. aulaca alaskana,

A. kupriyanovi, A. abyssalis 3460-5220 57-90

gitudinal) muscle layer of the proboscis wall. The retrac-
tors are always connected both with the proboscis walls
and the buccal tube by numerous muscle fibers.

The buccal tube leads from the buccal mass to the mouth
at the proboscis tip. In all species, the buccal tube is very
thin, semitransparent and is formed by one layer of epi-
thelial cells surrounded by a layer of circular muscles of
different thickness. The possibility cannot be excluded that
the buccal tube is capable of peristaltic movements. In all
Aforia species except A. circinata the buccal tube forms a
fold (sometimes double) directed backward along the buc-
cal mass walls. The functional significance of this fold
remains unclear. In its anterior part the buccal tube forms
an enlargement of various sizes surrounded by a sphincter
used for holding a single marginal tooth. The anterior part
of the proboscis is capable, at least in some species, of
introverting during contractions of the proboscis retractors.
This is most obvious in the morphology of the proboscis
tip in A. lepta and A. aulaca alaskana. Retraction of the
proboscis tip can be judged by the epithelium structure.
The anterior part of the buccal tube in these species has
the same kind of epithelium as the outer proboscis wall
(Figures 8B, 12G). However, at some distance from the
proboscis tip, the lining of the tube is as on the remainder
of the buccal tube. We believe that this change in epithelial
structure may be explained by introverting of the proboscis
tip.

The size of the usually powerful buccal mass is variable
in comparison with the proboscis length. The smallest
relative size of the buccal mass is in Aforia aulaca alaskana
and the largest is in A. kupriyanovt.

The boundary line between the back part of the buccal
mass and the oesophagus can be usually determined by
the place of an abrupt enlargement of the digestive tube
diameter near the opening of the poison gland. At that
region the thick layer of circular muscles that constitute
the major part of buccal mass wall becomes much thinner.

The radula is situated at the bottom of the buccal cavity.
The radular sac, containing the radula frontal part and
the odontophore, is connected with the buccal cavity through

The Veliger, Vol. 30, No. 2

a relatively long and narrow duct. All species except Aforia
lepta have more or less well developed odontophore car-
tilages. Aforza circinata, A. abyssalis, and A. moskalevi have
four cartilages which lie symmetrically, two on each side
of the odontophore. At the anterior part of the odontophore,
the cartilages of each pair join and a thick, muscular sym-
physis connects the two newly formed cartilages. The rad-
ula bends over this symphysis. Aforia crebristriata has only
two cartilages, which join in the anterior part of the odon-
tophore. This species also has the largest cartilages (Figure
10B). Aforia lepta lacks the cartilage tissue but has a thick
transverse muscle over which the radula bends. Relatively
good development of the odontophore and the muscles con-
nected with it seems to indicate that radular mobility is
sufficient to allow the odontophore to protrude into the
buccal cavity. The inner cavity of the anterior part of the
radular sac is lined with a thick cuticular layer which
prevents damage to the walls during radula movements.

The morphology of the radular marginal teeth was stud-
ied with the scanning electron microscope. Each tooth ap-
pears to consist of two parts or plates (Figures 3D, 4B-
D) which are free at the base of the tooth and flow together
at its tip. One of them has a thin ligament by which the
tooth is connected with the radular membrane. Sections of
the tooth show that in the proximal part both plates are
also connected with a cuticular membrane (Figure 4C).
The upper plate of the tooth is more rounded and the
lower one is crescent-shaped. These plates and the mem-
brane are differently stained by Mallory: the formers are
bright orange and the latter is dark blue. The plates and
membrane form a groove along both sides of the tooth.
The relative length of the marginal tooth (the shell height-
tooth length ratio) varies markedly among species, from
57 (A. kupriyanovt) to 180 (A. circinata). By comparing
this ratio with the bathymetric distribution of the species,
one can see that tooth length increases with the transition
from sublittoral to bathyal and to upper and lower abyssal
species (Table 2).

The poison gland is long, well developed, and powerful
in all species; it forms tight convolutions. The gland opens
approximately at the border between the buccal mass and
the oesophagus and rather distant from the opening of the
radular sac into the buccal cavity. This may indicate that
all of the inner cavity of the proboscis is filled with poi-
sonous liquid. The size of the muscular bulb varies: Aforia
lepta has the smallest one, A. abyssalis has the largest one,
and the muscular bulbs of A. crebristriata and A. moskalevi
are of medium size. All species have a rather small lumen
in the bulb, usually adjacent to the opening of the poison
gland. The walls of the muscular bulb are formed by two
layers of muscles, longitudinal and circular, which are not
separated by an intermediate layer of connective tissue as
in Conidae (HYMAN, 1967).

All Aforia species have large salivary glands situated
under the nerve ring. In A. circinata, A. moskalevi, and
A. crebristriata, the glands are united into a single mass.
The salivary ducts are always paired and weakly coiled.

A. V. Sysoev & Yu. I. Kantor, 1987

They open into a duct connecting the radular sac with the
buccal cavity. Proximal parts of the salivary ducts run
within the wall of the buccal cavity. Most parts of the
ducts are lined with a ciliary epithelium, which provides
transport for the gland secretion. As the duct opening is
approached, the ciliary epithelium is replaced by a smooth
one.

All Aforia species have differently developed rhyncho-
stomal lips, which are rounded muscular folds forming a
kind of funnel at the anterior side of the head. The rhyn-
chostome has a large powerful sphincter obviously used in
catching prey.

Other systems of organs of studied Aforia species are the
same as in other families of neogastropods. Morphology
of the mantle complex is similar in all species and is char-
acterized by substantial development of the gill and the
osphradium. The large sizes of the mentioned organs may
be conditioned by a low density of food resources at great
depths and by the necessity of an active mode of life. This
requires (1) high oxygen consumption, which is provided
by a large gill, and (2) the necessity of well-developed
chemoreception, which demands a considerable develop-
ment of the osphradium (KANTOR & SYSOEV, 1986).

Functional Analysis of Morphology
of the Digestive System

Recently, many authors have paid attention to morpho-
functional specializations of the digestive system of Tur-
ridae (SMITH, 1967; SHIMEK, 1975; SHERIDAN et al., 1973;
SHIMEK & KOHN, 1981). Most important is the exami-
nation of the anterior part of the digestive system and
radula, which are the most variable among turrids. Mor-
phological and functional types of turrid radulae were
analyzed by SHIMEK & KOHN (1981). According to the
classification proposed by those authors, Aforia, like other
representatives of the subfamily Turriculinae, has a slicing
radula used for tearing the prey body. The radulae of all
other Turridae, with well-developed subradular mem-
branes and mainly with “nontoxoglossate” solid marginal
teeth, are classified as slicing, slicing-rasping, and slicing-
stabbing types of radulae.

However, the functional types of ““nontoxoglossate”’ rad-
ulae and the correspondent mechanisms of functioning pro-
posed by Shimek & Kohn cannot explain many facts. The
buccal mass with radula is situated at the base of the
proboscis in all Toxoglossa and cannot be moved out through
the mouth as in other prosobranchiate gastropods. There-
fore, slicing the prey as supposed by Shimek & Kohn can
take place only in the buccal cavity after the prey is already
caught and partially swallowed. In this connection, the
presence of a well-developed, large poison gland in “‘non-
toxoglossan” Turridae cannot be explained, because en-
venomation of the prey inside the buccal cavity would seem
useless. On the other hand, the poison gland disappears
during reduction of the radula, and prey capture by species
with a reduced radula occurs with the help of proboscis

Page 123

or enlarged rhynchostomal lips (KANTOR & SYSOEV, 1986).
Using the classification of SHIMEK & KOHN (1981) it is
impossible to explain the functioning of such a specialized
radula as in Imaclava unimaculata (subfamily Clavinae)
which has true “‘toxoglossate” hollow marginal teeth along
with a central one and well-developed laterals. It is difficult
to imagine the mechanism by which poison would be passed
through the hollow marginal tooth or its usefulness, as
soon the buccal cavity would be filled with the poisonous
liquid. MAEs (1983) has also put forward reasonable doubts
about the slicing function of Clavinae radulae. She con-
sidered that the radula of Drillia cydia is used not for tearing
but for holding and perforating the prey, a fact confirmed
by finding almost intact polychaetes in the mollusk’s stom-
ach.

Thus, the hypothesis of a “slicing” or “slicing-stabbing”
function of turrid radulae possessing a well-developed sub-
radular membrane is not in agreement with many data.

In this connection, the findings of single marginal teeth
held by a sphincter of the proboscis tip in three Aforza
species (A. moskalevi, A. kupriyanovt, and A. abyssalis)
is of great interest. Morphology of the distal part of the
proboscis of other species also confirms the possibility that
the marginal tooth is held by the sphincter. The only
possible explanation of the fact is that marginal teeth,
removed from the subradular membrane in the sublingual
pouch during radular degeneration, are used at the pro-
boscis tip for stabbing prey and poisoning them with poi-
sonous liquid in a fashion similar (but not identical) to
that used in higher Toxoglossa. Grooves running along
both sides of the tooth (see above) could be used for ad-
ministering the poison. Thus, the radula of Aforia species
has two functions. The first is to stab the prey with the
single marginal tooth at the proboscis tip and to use the
radula as a whole in the buccal cavity. The second function
is to a great extent unclear for Aforza. It is possible that
the radula, which can move out to some extent into the
buccal cavity, is used to move the prey from the buccal
cavity to the oesophagus and probably for damaging the
prey tissues. In particular, this second function is confirmed
by the structure of the central tooth, which has one rather
large cusp on the frontal edge.

One can suppose that using the marginal teeth at the
proboscis tip is almost universal among turrids with a well-
developed subradular membrane. The fact is confirmed by
our finding of a marginal tooth at the tip of the proboscis
of Splendrillia sp. (subfamily Clavinae). The function of
the hollow marginal tooth of Imaclava unimaculata also
becomes obvious: the mollusk uses it at the proboscis tip
as higher Toxoglossa do.

Evolution of the radular apparatus is closely associated
with the evolution and morphology of the proboscis. SMITH
(1967) described a new type of proboscis of prosobranch
gastropods, an intraembolic one characterized by circular
folds formed by proboscis walls in their contracted state.
When describing the buccal apparatus of Oenopota levi-
densis, SHIMEK (1975) advanced the notion of the intraem-

Page 124

bolic proboscis and postulated that its principal feature
was the existence of a permanent rhynchodaeum; this means
that not the whole rhynchodaeum of the intraembolic pro-
boscis participates in the proboscis everting. However, in
many gastropods with a pleurembolic proboscis, even when
the proboscis is completley everted a part of the rhyncho-
daeum remains inside. A special subtype of pleurembolic
proboscis, the extraembolic type, was proposed for gastro-
pods in which the whole rhynchodaeum takes part in the
proboscis eversion and the proboscis sheath is absent dur-
ing the complete eversion of the proboscis (KANTOR, 1985).

Investigation of the proboscis morphology of several
species of Aforia allows us to state that all species of the
genus lack an invaginable part of the rhynchodaeum; that
is, everting of the proboscis results only from its stretching.
Comparison of Aforia with other turrids leads to a conclu-
sion that the main characteristics of the intraembolic pro-
boscis are the absence of the invaginable part of the rhyn-
chodaeum and the localization of the buccal mass at the
proboscis base.

Differences in the displacement of the buccal mass are
the most important differences between the intraembolic
and pleurembolic probosces as well as between rachiglos-
san and toxoglossan neogastropods in general. In fact, dur-
ing the origination of the proboscis by elongation of the
ancestral form snout, the elongation of the anterior oesoph-
agus in front of the nerve ring occurred in rachiglossan
families while elongation of the buccal tube connecting the
buccal cavity with the mouth occurred in toxoglossan groups
(PONDER, 1973). Thus, the two proboscis types have dif-
ferent origins and are not homologous. Formation of con-
centric telescopic folds within the walls of the intraembolic
proboscis serve to enhance its elongation.

The origin of the intraembolic type of proboscis may be
connected with the origin and development of the poison
gland. This process may be presented in the following way:
the poison gland that appeared in the toxoglossan ancestor
at the first stages of evolution was closely associated with
the radular apparatus. Probably the efficiency of the poison
gland and the poison itself was much lower than in modern
species. This required maximal proximity of the admin-
istered poison to the radula that was damaging the prey
tissue. At the same time elongation of the proboscis and
the appearance of the poison gland allowed “distant feed-
ing” on actively moving prey. Elongation of the proboscis
appears to be closely related to poison gland enlargement;
as the inner volume of the proboscis grew, more poison
was needed to fill it. Formation of a powerful poison gland,
which already did not fit the proboscis, prevented the gland
from everting together with the proboscis. At the same
time, distancing the radular apparatus from the opening
of the poison gland hampered the use of the poison. This
caused, in turn, fixation of the buccal mass at the proboscis
base. Most probably during that period of evolution the
mechanism developed of using marginal teeth at the pro-
boscis tip for stabbing the prey. Using the marginal teeth
at the proboscis tip did not require any considerable mor-
phological changes of the anterior part of the digestive

The Veliger, Vol. 30, No. 2

apparatus: in all prosobranch gastropods, the subradular
membrane degenerates in the sublingual pouch and worn
teeth are removed via the digestive tract. By contrast in
toxoglossan gastropods, teeth that separate from the sub-
radular membrane are transferred to the proboscis tip
where they were held by the sphincter. Using the single
tooth at the proboscis tip allowed a considerable elongation
of the proboscis because the function of stabbing the prey
was no longer associated with the radular apparatus per
se. Therefore, the appearance of the intraembolic proboscis
is associated with the appearance of the poison gland,
transition to “distant feeding” on actively moving animals,
and using the marginal tooth at the proboscis tip.

If the proposed scheme of evolution of the anterior diges-
tive apparatus is adopted, one can easily understand also
the appearance of the typically “toxoglossan” mode of
feeding as in higher Turridae and Conidae which possess
only hollow marginal teeth acting as a syringe needle. As
the proboscis elongated, the main radular function became
stabbing the prey with the individual tooth at the proboscis
tip. This led to reduction of the odontophore and, conse-
quently, of the subradular membrane. Thus, Aforza is a
kind of intermediate morphological stage transitional to
the typical “toxoglossate” forms. However, Aforia cannot
be considered as an intermediate evolutionary stage be-
cause modern turrids with a well-developed subradular
membrane often are more numerous than the typical tox-
oglossan forms; “nontoxoglossate” turrids should be con-
sidered as a result of evolution of a separate evolutionary
line (or lines), which is not the same as that resulting in
“true toxoglossates.” Probably, use of the radula not only
at the proboscis tip but also in the buccal cavity has some
advantages. If the radula were not used in the buccal cavity
it would be difficult to explain the existence of numerous
species of the subfamily Clavinae having, besides marginal
teeth, also central and large, powerful lateral teeth.

The mechanism of transporting the tooth from the rad-
ular sac to the proboscis tip in Aforia is presently unclear.
Pushing the tooth, separated from the membrane, into the
buccal cavity occurs probably by the contraction of the
powerful circular musculature of the radular sac. Trans-
portation of the tooth to the proboscis tip may occur along
with the flow of poisonous liquid during contraction of the
muscular bulb or also by peristaltic movements of circular
muscle fibers of the buccal tube. The position of the pro-
boscis sphincter and the length of the marginal tooth are
correlated so that the tooth, held at its base by the sphincter,
extends outside the proboscis. In this connection it is in-
teresting to analyze the morphology of the proboscis tip of
A. aulaca alaskana (Figure 12G). If one supposes that the
well-developed sphincter of the buccal tube is intended to
fix the tooth base, then the point of the tooth would not
protrude outside the proboscis. As has been mentioned
above, in this species, the proboscis tip can be everted and
after eversion the tooth point appears to be protruded out-
side. One can propose that such a mechanism was devel-
oped to protect the rhynchodaeum during eversion of the
proboscis with the already held tooth and also to protect

A. V. Sysoev & Yu. I. Kantor, 1987

Page 125

the tooth itself, as searching for prey is probably carried
out by a sense of touch of the proboscis tip. Transportation
of the tooth from the radular sac to the proboscis tip most
probably occurs at the moment of drawing the proboscis
into the rhynchodaeum because in this case the distance
from the buccal mass to the proboscis tip is much less than
that in the everted proboscis.

History of the Aforia Fauna

The genus under consideration is closest to the genera
Leucosyrinx Dall, 1889, Comitas Finlay, 1926, Parasyrinx
Finlay, 1924, and Turrinosyrinx Hickman, 1976. These
genera are apparently interrelated and have a common
ancestor.

The earliest certain findings of fossil species of Aforza
are known from the Oligocene. From the upper Oligocene
of northwestern North America, a rather diverse fauna of
Aforia, consisting of four species, has been recorded (Ja-
VIDPOUR, 1973). At present, a single finding of a Paleogene
species is known from the northwestern Pacific. The species
related to A. clallamensis (Weaver, 1916) was found, ac-
cording to unpublished data of V. N. Sinelnikova and A.
E. Oleynik, in deposits of western Kamchatka (Rategin
suite). However, dating of this suite currently is rather
uncertain (upper Eocene or upper Oligocene—A. E. Oley-
nik, personal communication).

Apparently the geographical center of the species di-
versity is the northern Pacific, with the most intensive
formation of species being in its northeastern region. This
is evident both from the relatively high diversity of fossil
Aforia species in this region and from the fact that the
highest morphological diversity of recent species is from
the Pacific coast of North America, the only region where
representatives of all the subgenera live.

Recent species of Aforia demonstrate an association with
low water temperatures, living generally in bathyal and
abyssal zones and rising into shallow waters only in high
boreal and Antarctic regions. One can confidently consider
that life in cold waters was characteristic of this genus
during all of its history and that adaptation to cold water
has conditioned the formative history of the recent fauna
of the genus.

The first Cenozoic phase of colder climates in the north-
ern Pacific began in the second part of the Eocene (Ka-
FANOV, 1982). Precisely in this period, formation of the
genus began. The temperature minimum was most pro-
nounced in the middle Oligocene (KAFANOV, 1982), and,
after achieving it, various and numerous upper Oligocene
Aforia fauna developed. However, some warming of the
climate in the northeastern Pacific began later in the Oli-
gocene (WOLFE & HopkKINs, 1967), reaching its maximum
in the northern Pacific at the end of the early or beginning
of the middle Miocene (KAFANOV, 1982). These facts are
well correlated with the disappearance of most of Afloria
species at the border between the Oligocene and Miocene
in fossil formations of the northwestern part of the U.S.A.,
with the single species being recorded at the very early

Miocene (JAVIDPOUR, 1973). Apparently this disappear-
ance was related to the leaving of Aforia species for bathyal
and abyssal regions of the northern Pacific. Representa-
tives of the deep-sea Miocene fauna are not known, but a
reason exists that forces us to consider that there was a
rather well-developed deep-sea fauna of Aforia in the Mio-
cene. At present there are two closely related species living
in the abyssal regions of the northern Pacific and northern
Atlantic respectively —A. abyssalis and A. hypomela. Ob-
viously these two species are relicts of the early Miocene
deep-sea fauna of Central America. Geographical sepa-
ration of the species resulted from the forming of the central
American isthmus and the closing of the deep-sea connec-
tion between the Pacific and the Atlantic, which are dated
to the middle Miocene (for a review of this subject see
NEsIS, 1985).

One can suppose that, precisely in the Miocene, migra-
tions of bathyal species began southward along the Pacific
coast of North and South America. Similar migrations have
been reconstructed in the geological history of many other
groups of animals (NEsIs, 1985). Presently, the movement
of Aforia representatives southward is traced by the dis-
tribution of recent bathyal and abyssal species and sub-
species from the eastern Pacific (POWELL, 1951; present
data).

The late Miocene Nuvok transgression (KAFANOV, 1982)
has led to the forming of a connection between the north
Pacific and Polar basins, which in turn caused a cooling
of the climate. In this respect, a gradual rising of Aforia
species to more shallow zones, including the western Pa-
cific, began during the Pliocene. An earlier Pliocene finding
of Aforia is recorded from the Tomya Formation of Honshu
(OTuUKA, 1949) which is characterized by a relatively deep-
sea (bathyal) fauna (OKUTANI, 1968). Also at the Pliocene
A. circinata appears on the shelf of the Gulf of Alaska
(JAVIDPOUR, 1973) and in deposits of eastern Kamchatka
(PETROV, 1982). Thus, just at the Pliocene, the fauna of
Aforia obtained its principal features of its Recent ap-
pearance and distribution.

The rising of a part of the species to shallow but cold
zones took place also in the southern Pacific. Some Ant-
arctic species that migrated from the northern Pacific along
the American coast have settled in the shallow zone for a
second time, rising up to the sublittoral. The rising of
Aforia species to shallow waters in Antarctic regions, while
species distributed in tropical and subtropical latitudes
retained their relation within deep-sea habits, has been
analyzed in detail by POWELL (1951).

Presently the main part of Aforia species live in the
Pacific, being distributed almost circumoceanically except
for the western Pacific (Rukue Islands at the north to
Macquarie Island at the south). A single species (A. hy-
pomela) is recorded from the northern Atlantic and two
species (A. gonioides and A. magnifica) penetrate into the
southwestern Atlantic. Another two species penetrate also
into the southern part of the Indian Ocean (A. lepta and
A. staminea). Most species show a near-continental dis-
tribution.

Page 126

The Veliger, Vol. 30, No. 2

ACKNOWLEDGMENTS

We wish to express our cordial thanks to Dr. L. I. Mos-
kalev and V. Ya. Lus (Institute of Oceanology of the
U.S.S.R. Academy of Sciences) and to Dr. V. N. Gorya-
chev (Zoological Museum of Moscow State University)
for their kind assistance in access to material for study.
An incalculable help in carrying out the histological study
was given to us by Dr. S. Kupriyanov (Institute of General
Genetics of the U.S.S.R. Academy of Sciences) and Dr. S.
V. Saveljev (Institute of Human Morphology of the
U.S.S.R. Academy of Sciences). We are also greatly in-
debted to Dr. V. N. Sinelnikova and A. E. Oleynik (Geo-
logical Institute of the U.S.S.R. Academy of Sciences) for

consultations on fossil species.
We also wish to thank Dr. David W. Phillips, Editor
of The Veliger for assistance with the manuscript.

LITERATURE CITED

BarTSCH, P. 1945. The west Pacific species of the molluscan
genus Aforia. Jour. Wash. Acad. Sci. 35(12):388-393.
BoucHET, P. & A. WAREN. 1980. Revision of the north-east
Atlantic bathyal and abyssal Turridae (Mollusca, Gastro-

poda). Jour. Moll. Stud. Suppl. 8:1-119.

CANTERA, J. R. & P. M. ARNAUD. 1984. Les Gasteropodes
Prosobranches des iles Kerguelen et Crozet (sud de l’ocean
Indien). Comparaison ecologique et particularities biolo-
giques. Comit. Nat. Franc. Rech. Antarct. 56:1-169.

CERNOHORSKY, W. O. 1972. Comments on the authorship of
some subfamilial names in the Turridae. Veliger 15(2):127-
128.

DALL, W. H. 1896. Diagnoses of new species of mollusks from
the west coast of America. Proc. U.S. Natl. Mus. 18(1034):
7-20.

DaLL, W. H. 1908. Reports on the dredging operations off the
west coast of Central America to the Galapagos ....
XXXVIII. Reports on the scientific results of the expedition
to the eastern tropical Pacific .... XIV. Reports on the
Mollusca and Brachiopoda. Bull. Mus. Compar. Zool. 43(6):
205-487.

GranT, U.S. & H. R. Gate. 1931. Catalogue of the marine
Pliocene and Pleistocene Mollusca of California and adjacent
regions. Mem. San Diego Soc. Natur. Hist. 1:477-612.

Hickman, C. 8. 1976. Bathyal gastropods of the family Tur-
ridae in the early Oligocene Keasey formation in Oregon
with review of some deep-water genera in the Paleogene of
the eastern Pacific. Bull. Amer. Paleontol. 70(292):1-119.

Hyman, L. H. 1967. The Invertebrates. Vol. 6: Mollusca I—
Aplacophora, Polyplacophora, Monoplacophora, Gastro-
poda. McGraw-Hill Book Co.: New York. 792 pp.

Javippour, M. 1973. Some records on west American Cenozoic
gastropods of the genus Aforia. Veliger 15(3):196-205.

KaFANov, A. I. 1982. Cenozoic history of malacofauna of the
north Pacific shelf. Pp. 134-175. Jn: Marine biogeography.
Nauka: Moscow [in Russian].

Kantor, YU. I. 1985. Feeding and some features of functional
morphology of the molluscs in the subfamily Volutopsiinae
(Gastropoda, Pectinibranchia). Zool. Zhurn. 64(11):1640-
1647 [in Russian].

KanTor, Yu. I. & A. V. SysoEv. 1986. New species of the
family Turridae from the northern part of the Pacific ocean.
Zool. Zhurn. 65(4):485-498 [in Russian].

Mags, V.O. 1983. Observations on the systematics and biology
of a turrid gastropod assemblage in the British Virgin Is-
lands. Bull. Mar. Sci. 33:305-335.

McLEan, J. H. 1971. A revised classification of the family
Turridae, with the proposal of new subfamilies, genera and
subgenera from the eastern Pacific. Veliger 14(1):114-130.

McLean, J. H. 1971. Family Turridae. Pp. 686-766. In: A.
M. Keen, Sea shells of tropical West America, marine mol-
lusks from Baja California to Peru. 2nd ed. Stanford Univ.
Press: Stanford, California.

NesIs, K. N. 1985. Oceanic cephalopod molluscs. Nauka: Mos-
cow. 286 pp. [in Russian].

OxkuTANI, T. 1968. Systematics, ecological distribution and pa-
laeoecological implication of archibenthal and abyssal Mol-
lusca from Sagami Bay and adjacent areas. Jour. Fac. Sci.,
Univ. Tokyo, sect. II 17(1):1-98.

OtuKa, Y. 1949. Fossil Mollusca and rocks of the Kigosumi
group exposed at Minato-machi, Chiba Prefecture, and its
environs (lst paper). Japan. Jour. Geol. Geogr. 24(1-4):
295-309.

PARKER, R. H. 1964. Zoogeography and ecology of some mac-
ro-invertebrates, particularly mollusks, in the Gulf of Cal-
ifornia and continental slope off Mexico. Viddensk. Medd.
Dansk. Naturh. Foren 126:1-178.

Petrov, O. M. 1982. Marine molluscs of the anthropogene
from the northern region of the Pacific. Trudy Geologi-
cheskogo in-ta AN SSSR (Proc. Geol. Inst. USSR Ac. Sci.)
357:1-143 [in Russian].

PONDER, W. F. 1973. Origin and evolution of the Neogastro-
poda. Malacologia 12(2):295-338.

PowELL, A. W. B. 1942. The New Zealand recent and fossil
Mollusca of the family Turridae with general notes on turrid
nomenclature and systematics. Bull. Auckland Inst. Mus. 2:
1-192.

PowELL, A. W. B. 1951. Antarctic and subantarctic Mollusca.
Pelecypoda and Gastropoda. Discovery Rept. 26:47-196.

PowELL, A. W. B. 1966. The molluscan families Speightiidae
and Turridae. Bull. Auckland Inst. Mus. 5:1-184.

POWELL, A. W. B. 1969. The family Turridae in the Indo-
Pacific. Part 2. The subfamily Turriculinae. Indo-Pacific
Mollusca 1(7):207-416.

Roxop, F. J. 1972. Notes on abyssal gastropods of the eastern
Pacific, with description of three new species. Veliger 15(1):
15-20.

SHERIDAN, R., J.-J. VAN MoL & J. BouILLoN. 1973. Etude
morphologique du tube digestif de quelques Turridae (Mol-
lusca—Gastropoda—Prosobranchia—Toxoglossa) de la re-
gion de Roscoff. Cah. Biol. Marine 14:159-188.

SHIMEK, R. L. 1975. The morphology of the buccal apparatus
of Oenopota levidensis. Ztr. Morphol. Tiere 80:59-96.
SHIMEK, R. L. & A. J. KOHN. 1981. Functional morphology
and evolution of the toxoglossan radula. Malacologia 20(2):

423-438.

SMITH, E. H. 1967. The proboscis and oesophagus of some
British turrids. Trans. Roy. Soc. Edinburgh 67(1):1-22.
WATSON, R. B. 1881. Mollusca of H.M.S. “Challenger” ex-

pedition. Part 8. Jour. Linn. Soc. 15:388-412.

WATSON, R. B. 1886. Reports on the Scaphopoda and Gas-
tropoda collected by H.M.S. “Challenger” during the years
1873-76. Rept. Sci. Res. Challenger Exped., Zool. 42:1-
756.

WoLFE, J. A. & D. M. Hopkins. 1967. Climatic changes
recorded by Tertiary land floras in northwestern North
America. Pp. 67-76. Jn: Proc. 11th Pacific Sci. Congr., Symp.
25. Tokyo, 1966. Sasaki: Sandai.

The Veliger 30(2):127-133 (October 1, 1987)

THE VELIGER
© CMS, Inc., 1987

The Effects of Aggregation and Microhabitat on

Desiccation and Body ‘Temperature of the Black ‘Turban
Snail, Zegula funebralis (A. Adams, 1855)

by

KAREN E. MARCHETTI

University of California, Bodega Marine Laboratory, Box 247, Bodega Bay, California 94923, U.S.A.

AND

JONATHAN B. GELLER!

Bodega Marine Laboratory’, Box 247, Bodega Bay, California 94923, U.S.A. and
Department of Zoology, University of California, Berkeley, California 94720, U.S.A.

Abstract.

We studied the roles of aggregative behavior and microhabitat differences in reducing

desiccation of the rocky intertidal prosobranch gastropod Tegula funebralis (A. Adams, 1855) at Bodega
Bay, California. Solute concentration of extra-corporeal water (ECW) was measured as an indication
of desiccation through evaporative water loss. In the majority of field collected samples, aggregated
Tegula funebralis had lower ECW solute concentrations than solitary individuals. In laboratory exper-
iments, smaller individuals desiccated faster. In the field, microhabitats had a large influence on des-
iccation stress: both aggregated and solitary individuals in protected microhabitats during times of
exposure had lower solute concentrations than individuals in exposed microhabitats. Microhabitat
differences had no effect on body temperature, but aggregated snails were significantly cooler.

INTRODUCTION

Organisms inhabiting the rocky intertidal zone are con-
tinuously subject to a variety of physical stresses. During
each tidal cycle, these organisms may be subject to con-
ditions of essentially a terrestrial environment (DAVIES,
1969; VERNBERG & VERNBERG, 1972). Evaporative water
loss upon exposure to wind and solar radiation may result
in high levels of desiccation. Behavioral and physiological
adaptations to desiccation are therefore important for sur-
vival in the rocky intertidal environment (GARRITY, 1984).

The purpose of this study was to investigate the effects
of aggregative behavior on desiccation and body temper-
ature in Tegula funebralis (A. Adams, 1855), and some of
the factors influencing this behavior. Tegula funebralis, the
black turban snail, isa common middle intertidal gastropod

' Author for correspondence.
? Address for correspondence.

occurring from Vancouver Island, British Columbia, to
Central Baja California (Morris et al., 1980). Although
its spatial distribution has been studied (see, for example,
WARA & WRIGHT, 1964; PAINE, 1969; FAWCETT, 1984),
little attention has been given to the aggregative behavior
of this species and its possible role in reducing desiccation
stress.

We examined this question by comparing extra-cor-
poreal water (ECW) samples from aggregated and solitary
snails. Extra-corporeal water, held within the mantle cav-
ity, is a source of evaporative water loss in exposed snails.
Wo cotTtT (1973) showed that, for limpets, mortality dur-
ing low tide exposure is associated with concentration of
internal fluids resulting from evaporative water loss.

Microhabitat choice by snails may also play an impor-
tant role in avoiding desiccation (GARRITY, 1984). It was
therefore our further intent to investigate the relative im-
portance of aggregation and microhabitat selection in re-
ducing desiccation stress.

Page 128

1500

1400

W
(eS)
Oo

1200

eel

1000 +

BLOOD OSMOLARITY
(mOSM/Kg)

900 + t +
900 1000 1100

The Veliger, Vol. 30, No. 2

V=0.959X 1397.82

aa

iZOe 1300 1400 1500

ECW OSMOLARITY (mOSM /Kg)
Figure 1

Relationship between blood osmolarity and extra-corporeal water osmolarity in Tegula funebralis. The plotted line

and equation are the linear regression of these variables.

MATERIALS anpD METHODS

This study was conducted during April and May 1986,
on the Bodega Marine Life Reserve, Sonoma County,
California. Laboratory studies were conducted at the Bo-
dega Marine Laboratory. Field data were collected during
low tides, at a tidal level of approximately 1.5 m above
mean lower low water. Temperature, wind conditions, and
time of day differed during collection of field data, but
conditions were qualitatively similar. The substratum was
heterogeneous, consisting of bare flat rock, crevices, and
various degrees of algal cover (mainly Endocladia muricata
[Postels and Ruprecht, 1840], Pelvetiopsis limitata Gard-
ner, 1910, and Porphyra sp.). SUTHERLAND (1970) and
WOLCOTT (1973) provide further details of the study site.

Field Studies

To use ECW as a measure of desiccation, it was first
necessary to determine that Tegula funebralis is isoosmotic
with its aqueous environment, and that osmolarity of in-
ternal fluids increases with increasing osmolarity of ECW.
To confirm this relationship, we collected snails from the
field and placed them in the sun for various lengths of
time. This allowed testing over a wide range of evaporative
water loss. Extra-corporeal water samples were collected
by pressing lightly on the operculum with a capillary tube
(0.9 mm diameter), allowing a small amount of ECW to
be drawn into the tube as the snail withdraws and ECW
is forced out of the mantle cavity. Capillary tubes were
immediately plugged with plasticene clay, to prevent fur-
ther evaporation of samples.

Blood samples were taken by removing individuals from

their shells, pat-drying any residual ECW, and cutting the
foot with a razor blade. A blood sample large enough for
analysis could then be drawn by placing a small capillary
tube (0.5 mm diameter) into the laceration and applying
pressure to the foot. For each snail, 8 wL samples of both
blood and ECW were analyzed using a Wescor 5130 C
vapor pressure osmometer. Solute concentration (osmo-
larity) was measured in milli-osmoles per kilogram (mOsm/
kg) blood or ECW.

Extra-corporeal water was sampled in the field in order
to compare differences in extent of desiccation between
aggregated and solitary Tegula funebralis. Sampled aggre-
gations always consisted of at least 10 individuals, each in
contact with at least one other snail. In the first trials,
solitary individuals sampled were always within 30 cm of
a given sampled aggregation, and at least 5 cm away from
any other snail, following the criteria of GALLIEN (1985).
This procedure assured that aggregated snails and sur-
rounding solitary snails were from the same microhabitat.
Seven sets of aggregations and nearby solitary snails were
sampled. As a measure of size, the greatest shell width was
recorded for each individual.

A second set of field samples tested the effect of micro-
habitat on level of desiccation. Extra-corporeal water sam-
ples were taken from snails within two distinct microhab-
itats: exposed (bare rock with no crevices) and protected
(containing crevices and[or] algal cover). Temperatures of
all individuals in the second field sampling were also mea-
sured using a Keithly 870 K-type thermocouple thermom-
eter. The probe was placed against the foot, and the snail
was allowed to retract into its shell, pulling the probe into
the mantle cavity. Snails were in contact with only the

K. E. Marchetti & J. B. Geller, 1987

Table 1

Two-way analysis of variance testing the effects of differ-

ent field sites and aggregation on extra-corporeal water

soluteconcentration in 7egulafunebralis. (Significance levels:
HAP << OMe "12 << OMCs)

Source SS DF MS F-ratio
Site 59,640.2 6 9940.0 Qe
Aggregation 92,685.1 1 92,685.1 ED) PRC
Site x

aggregation 64,878.2 6 10,813.0 SA

probe for the duration of the reading, with minimal contact
with fingers which may warm the snail.

Laboratory Studies

The effect of aggregative behavior on decreasing des-
iccation stress was also examined in the laboratory. Ar-
tificial aggregations consisted of seven snails, five of which
were randomly chosen to be sampled for ECW. Both sol-
itary snails and artificial aggregations of small (9-12 mm)
and medium sized (16-18 mm) snails were placed in 4-cm
diameter cells in a plastic tray while being desiccated.
Owing to their size, solitary snails and artificial aggre-
gations of large (22-25 mm) snails were placed in larger
4.5 x 5.5-cm rectangular cells while desiccating. Snails
were restrained in cells by a cover of 10-mm mesh nylon
netting. Snails were desiccated under two lightbulbs (75
and 100 W) situated 35 cm almost vertically above them.
Air was moved over the snails by placing a household
electric fan 65 cm vertically above them. Ten aggregated
individuals and 10 solitary individuals were sampled every
hour for six hours. Measures of osmolarity and temper-
atures were recorded as an indication of level of desiccation
stress. A different set of snails was used for each period
of time.

Stress resulting from desiccation was assayed in a second
group of snails (all 16-18 mm; desiccated for 4, 6, and 8
hr) by measuring the amount of time necessary for the
individual to fully emerge from its shell, adhere to the
container, and resume function of cephalic tentacles upon
rehydration in normal seawater. For brevity, this behavior
is henceforth referred to as emergence. Osmolarity of ECW
was sampled before testing for time of emergence: these
values were used as a further measure of desiccation.

Behavioral Tests

We examined two potential cues that may be involved
in the aggregative behavior of Tegula funebralis. First, in
order to determine possible preference for light or dark
substrata, eight snails were placed uniformly (one per
square; see below) in a 19 x 30 x 4-cm pan containing
a checkerboard pattern of alternating black and white 9 x
5-cm squares. Locations of snails were noted after 30 min

Page 129

Table 2

Analyses of covariance (snail size as covariate) testing the
effects of aggregation and snail size on desiccation of Tegula
funebralis as measured by solute concentration of extra-
corporeal water. Snails were measured in seven sites on
two consecutive days. Differences in slope for aggregated
and solitary snails were tested before ANCOVA was per-
formed: slopes within sites were not different except for
site 6. (Significance levels: * P < 0.05; ** P < 0.01; ns,

P > 0.05.)
Source SS DF MS F-ratio

Site 1
Aggregation 1396.3 1 1396.3 0.55ns
Size 2160.7 1 2160.7 0.86ns
Residual 68,005.9 = 27 2518.7

Site 2
Aggregation 52,285.0 52,285.0 6.14*
Size 9707.7 1 9707.7 1.14ns
Residual 136,293.9 16 8518.4

Site 3
Aggregation 2889.4 1 2889.4 5.67*
Size 108.7 1 108.7 0.21ns
Residual 11,210.2 22 509.6

Site 4
Aggregation 7093.9 1 7093.9 2.36ns
Size 11,762.1 1 11,762.1 3.91ns
Residual S29) 1 3006.6

Site 5
Aggregation 14,858.6 1 14,858.6 8.84**
Size 648.6 1 648.6 0.39ns
Residual 36,995.6 22 1681.6

Site 6
Aggregation 41,234.5 1 41,234.5 2304 oe
Size 27,555.8 1 27,555.8 15:67 *
Aggregation x

size 23,625.8 1 23,625.8 Brae

Residual 38,746.9 22 1761.2

Site 7
Aggregation 16,576.2 1 6576.2 6.6*
Size 8825.9 1 8825.9 3.5ns

(little movement was observed after this period). Twenty
trials of this test were performed, and each individual snail
was tested only once.

Secondly, we examined the role of mucus trail following
in the formation of aggregations. The following experiment
tested whether snails will choose to follow a conspecific
mucus trail regardless of substrate color, or move to dark
substrata regardless of the presence or absence of a mucus
trail. Mucus trails were created by allowing one snail to
move freely on a 19-cm diameter clear plastic sheet placed
in a 19-cm petri dish divided into four equal-sized alter-
nating black and white quadrants. This plastic disk could
then be rotated such that the trail led to a white or a black

Page 130

1300 + fe)
T
1250+ fo)

| ZOO --

4

1 1505p

1100+

1050+
|

The Veliger, Vol. 30, No. 2

a Sie ee

12505
it

ECW OSMOLARITY (mOSM/Kg)

+—+—+—+

{$+ 3+ —+$- —}- +++ $$ +_$_ +_ +—_

@ 000
e e
1 OOO +--+ 4 4
5 10

SIZE (ran)

Figure 2

Relationship between snail size and osmolarity of extra-corporeal water of aggregated snails (solid circles and
bottom line) and solitary snails (open circles and top line) snails. In site 6 (top graph), slopes are significantly
different; in site 7 (bottom graph), slopes are not different but solitary snails are significantly more desiccated (see

Table 2).

quadrant. For each mucus trail, a second snail was tested
with the trail leading to a dark quadrant, and a third snail
was tested with the trail leading to a white quadrant. This
procedure was repeated 24 times.

RESULTS
Field Studies

The validity of extra-corporeal water as an indirect
measure of blood concentration, and therefore desiccation,
was confirmed (Figure 1). Results of a linear regression
revealed that solute concentration (Y) of blood increased
with that of ECW (X) (7 = 0.83; Y = 0.935X + 157.82;
n = 18, P < 0.001).

A preliminary two-way analysis of variance (ANOVA)
of the results from the first field samples indicated signif-
icant differences in solute concentration among the seven
sites and between solitary and aggregated individuals (Ta-
ble 1). For easier interpretation, separate analyses of co-
variance (ANCOVA) were performed for each site, with
snail size as the covariate. The results of these analyses
are presented in Table 2, and representative data are shown

in Figure 2. In two of the seven sites (sites 1 and 4), there
were no significant differences in ECW solute concentra-
tion between aggregated and solitary snails, nor any re-
lationship to snail size. In four of the seven sites (sites 2,
3, 5, 7), ECW solute concentration differed significantly
between aggregated and solitary snails, but again had no
relationship to snail size. In one site (site 6), the slopes of
the regression lines for aggregated and solitary snails dif-
fered: inspection of the data (Figure 2) indicates that in
this site, differences in osmolarity between aggregated and
solitary snails vary with snail size, with solitary snails
more desiccated and this difference most pronounced for
small snails. It should be noted that in all seven sites, the
slopes of regression lines relating snail size to ECW solute
concentration were always negative, but significantly so
only in site 6.

The results of the second field trials, which considered
microhabitat as well as aggregation, indicated that the
effect of microhabitat on desiccation is also important (Fig-
ure 3). A two-way ANOVA showed that the effect of
microhabitat (protected vs. exposed) on ECW concentra-
tion was highly significant (F5; = 33.40; P < 0.001),

K. E. Marchetti & J. B. Geller, 1987

ae =
“— @ ina a
a 25 Fj a Ss bs
Ww je) KE = =e
7) << fo) oO
Lo (2) n li
ow we te
5 20 io ©
5 g :
a
a
= 15
i
K-_
10
>
a
2007 < a
SS T a &
= o S
A tisost eo a
= [o) oS =
[e) o <<
e 1100 + 5 oe
ool ;
©) 10504
=
Y +
oO I
1000
EXPOSED PROTECTED
Figure 3

Temperatures (top graph) and extra-corporeal water osmolarity
(bottom graph) of solitary and aggregated Tegula funebralis in
protected (crevices or algal cover) and exposed (open surfaces)
microhabitats. Temperature did not differ between microhabitats,
but aggregated snails were significantly cooler. Osmolarity was
lower in protected microhabitats, but solitary and aggregated
snails did not differ.

while in this case the effects of aggregation and the inter-
action between aggregation and microhabitat were not sig-
nificant (aggregation: F, = 3.29; 0.08 > P < 0.05; in-
teraction: F,,, = 2.60; P > 0.1). In these trials, both
aggregated and solitary snails in protected habitats sus-
tained lower levels of evaporative water loss than did ag-
gregated or solitary snails in exposed microhabitats: mean
values (+SD) for protected microhabitats were 1048
38 mOsm/kg (n = 24) and 1050 + 40 mOsm/kg (n
25) for aggregated and solitary snails, respectively; for
exposed microhabitats, mean values were 1090 + 26
mOsm/kg (n = 23) for aggregated snails and 1125 + 78
mOsm/kg (n = 25) for solitary snails (Figure 3).
Protective cover had no significant effect on snail body
temperature (Figure 3). A two-way ANOVA showed no
significant effect of microhabitat (exposed vs. protected)
(F5; = 1.26; P > 0.26), while aggregated snails were
significantly cooler than solitary snails (F, 5; = 229.67; P <
0.001). There was also a significant interaction between
aggregation and microhabitat (F,,, = 11.51; P < 0.01):
inspection of the data indicates that the difference between
aggregated and solitary snails is greatest in exposed mi-

| the

Page 131

Table 3

Two-way analysis of covariance (time of exposure as co-
variate) testing the effects of time of exposure, snail size,
and aggregation on desiccation of Tegula funebralis as mea-
sured by solute concentration of extra-corporeal water.
(Significance levels: * P < 0.05; *** P < 0.001; ns, P >

0.05.)

Source SS DF MS F-ratio
Aggregation 52,586.5 1 52,586.5 3.46ns
Snail size 103,725.6 2 51,862.8 3.41*
Time of

exposure 4,428,927.7 1 4,428,927.7 291.48***
Aggregation x

snail size 20,184.6 2 10,092.3 0.66ns
Aggregation Xx

time 39,440.5 1 39,440.5 2.60ns
Snail size x

time 527,567.2 2 263,783.6 IES ORs

Aggregation x

snail size x

time 33,544.3 2
Residual 4,862,293.4 320

16,772.1 1.10ns
15,194.7

crohabitats (Figure 3). Mean body temperatures (+SD)
for aggregated snails were 17.2 + 1.0°C in protected mi-
crohabitats and 16.3 + 0.5°C in exposed microhabitats.
For solitary snails, mean body temperatures were 20.3 +
1.3°C (protected) and 20.7 + 1.7°C (exposed). In addition
to reducing evaporative water loss, as shown above, ag-
gregative behavior may be a means of reducing body tem-
perature.

Laboratory Studies

Results from the laboratory agreed with those from the
field, further supporting the hypothesis that aggregative
behavior reduces desiccation stress. For all size classes
combined over all time periods (1-6 h), solitary snails had
higher osmolarity of ECW than aggregated snails (F264 =
19.49; P < 0.001). A more detailed two-way ANCOVA
(Table 3) (time as the covariate) indicates significant effects
of time and snail size on ECW concentration (P < 0.05)
and a near significant effect of aggregation (P = 0.064):
under laboratory conditions, time of exposure appeared to
have the greatest effect on desiccation. The only significant
interaction in the three-way ANOVA was that of time
and snail size (Table 3). This can be interpreted as a
proportionally greater effect of time of exposure on small
snails than on large snails.

Desiccation affected time for emergence: two separate
one-way ANCOVAs, with aggregation as the main factor
and time of exposure or final osmolarity as the covariate,
showed that both time of exposure and osmolarity of ECW
had significant effects on time for snails to emerge from
their shells following rehydration (time: F,5, = 43.85; P <
0.001; osmolarity: F\5, = 53.75; P < 0.001). In neither
case did aggregation significantly effect time for emergence

Page 132

(0.09 > P > 0.05), nor were there significant interaction
terms.

Behavioral Tests

When snails were placed on a substratum with a check-
erboard pattern of black and white squares, six or more
of the eight snails were found to situate themselves on
black squares in 18 of the 20 trials performed. Using this
conservative criterion for preference (that is, six or more
of eight snails), a chi-square test indicates that this result
is significantly different from an null hypothesis of even
frequency of preference for black or white (x* = 12.8, df =
il, P< OOO).

In the experiment testing the role of mucus trails, snails
placed on a mucus trail leading to a black quadrant went
to a black quadrant 21 times, while 3 snails went to a
white quadrant. This differs significantly from a random
distribution (x? = 13.5, df = 1, P < 0.001). This first test,
however, does not differentiate between preference for a
black substratum vs. trail following. In the second test,
most (21 of 24) of the disks had one or two mucus trails
(depending on the path taken by individual snails) leading
to a black quadrant. When the disk is rotated one quarter
turn, these trails lead to white quadrants. If mucus trail
following is of primary importance, the null hypothesis is
that all of the snails should have followed a trail to a white
quadrant. Instead, all 24 snails went to a black quadrant,
and a chi-square test (confined to these 21 snails) rejects
this null hypothesis (x? = 21, df = 1, P < 0.001).

DISCUSSION

This study suggests that aggregative behavior in Tegula
funebralis may be of importance in reducing desiccation
stress. Aggregated snails in the laboratory and in the field
were shown to lose less water after a given period of time
desiccated than solitary snails. In addition, although ECW
concentration and not aggregation per se significantly af-
fected the time taken for emergence, aggregated snails un-
der field conditions should resume normal activity more
rapidly than solitary snails owing to the correlation be-
tween aggregation and extent of desiccation. Previous stud-
ies on different organisms support the conclusion that ag-
gregative behavior reduces desiccation stress. WARBURG
(1968) showed that aggregated terrestrial isopods lost water
at one-half the rate of solitary individuals owing to a re-
duction in exposed surface area-to-volume ratio. SNy-
DER-CONN (1980) demonstrated enhanced survivorship of
aggregated hermit crabs under desiccating conditions. For-
mation of aggregations reduces water loss and enhances
survivorship in a tropical neritid (GARRITY, 1984; GARRITY
& LEVINGS, 1984). Many studies have indicated that des-
iccation rates increase with decreased body size (see, for
example, Davigs, 1970; WOLCOTT, 1973). Our observa-
tions agree with these findings: small snails desiccated
significantly faster than large snails regardless of aggre-
gated or solitary conditions.

The Veliger, Vol. 30, No. 2

Aggregation may also be a means of regulating body
temperature, and therefore metabolic rate, while exposed.
In many invertebrates, metabolic rate varies with changes
in salinity and(or) temperature. The ability to withstand
a short-term rise in ambient temperature or salinity with-
out a significant rise in metabolic rate may be essential to
the maintenance of energetic gain in organisms that ex-
perience variable environmental temperatures and reduced
food availability upon exposure (NEWELL, 1979). Aggre-
gated Tegula funebralis in different microhabitats (pro-
tected or exposed) had similar temperatures, and these
temperatures were lower than those of solitary snails in
either microhabitat. This may be due to water held be-
tween individuals, thereby keeping snails at a more con-
stant and lower temperature.

It is of interest to determine whether aggregative be-
havior functions primarily as a means of reducing desic-
cation, or whether aggregations are formed as a result of
snails converging into protected areas upon exposure. Sev-
eral observations from this study suggest that aggregations
in protected microhabitats may be formed artifactually,
owing to crowding into protected areas, while those in
exposed microhabitats may be formed actively, owing to
orientation toward other snails. First, differences in des-
iccation stress (due to evaporative water loss) were found
to be largest between aggregated and solitary snails in
exposed microhabitats, but were not found to exist between
aggregated and solitary snails in protected microhabitats.
That is, desiccation stress in solitary individuals in exposed
microhabitats is relatively high, and a behavior for reduc-
ing this stress would be advantageous. Second, our labo-
ratory investigation of preference for dark-colored vs. light-
colored substrata indicates strong directionality toward dark
areas of the substratum, potentially a cue for protective
cover. Third, mucus trails seem to be of little importance
to snails in the formation of aggregations: snails did not
follow trails leading to white areas of the substratum.
Therefore, cues indicative of protective cover may be of
greater importance to exposed snails than cues indicating
the presence of other snails. In the absence of protective
cover, snails may orient to other snails with the dark shell
as a primary cue.

The results of this study show that aggregation is an
effective method for reducing desiccation stress due to evap-
orative water loss. Microhabitat choice also appears to be
an effective method, however, and the question as to wheth-
er aggregations are formed as a means of reducing desic-
cation or as a result of crowding into protected microhab-
itats upon exposure during low tide may have more than
one answer. In unprotected microhabitats, snails may ac-
tively seek to form aggregations. In protected microhabi-
tats, aggregations may be the result of a common orien-
tation toward cues representing protective cover.

ACKNOWLEDGMENTS

We wish to thank V. Chow, P. Connors, C. Declerck, B.
Kraus, C. Petersen, and T. Suchanek and two anonymous

K. E. Marchetti & J. B. Geller, 1987

reviewers for helpful advice, discussions and(or) comments
on the manuscript. We also thank Director J. Clegg and
the staff of the Bodega Marine Laboratory for making
facilities there available.

LITERATURE CITED

DaviEs, P. S. 1969. Physiological ecology of Patella. III. Des-
iccation effects. Jour. Mar. Biol. Assoc. U.K. 49(2):291-
304.

Davies, P. S. 1970. Physiological ecology of Patella. IV. En-
vironmental and limpet body temperatures. Jour. Mar. Biol.
Assoc. U.K. 50:1069-1077.

Fawcett, M. H. 1984. Local and latitudinal variation in pre-
dation on an herbivorous marine snail. Ecology 65(4):1214-
1230.

GALLIEN, W. B. 1985. The effect of aggregations on water loss
in Collisella digitalis. Veliger 28(1):14-17.

Garrity, S. D. 1984. Some adaptations of gastropods to phys-
ical stress on a tropical rocky shore. Ecology 65(2):559-574.

Garrity, S. D. & S. C. LEvinGs. 1984. Aggregation in a
tropical neritid. Veliger 27(1):1-6.

Morris, R. H., D. P. ABBotTT & E. C. HADERLIE. 1980. In-

Page 133

tertidal invertebrates of California. Stanford University Press:
Stanford, California. 690 pp.

NEWELL, R. C. 1979. Biology of intertidal animals. Marine
Ecological Surveys LTD. 781 pp.

PAINE, R. T. 1969. The Pisaster-Tegula interaction: prey patches,
predator food preference, and intertidal community struc-
ture. Ecology 50(6):950-961.

SNYDER-Conn, E. K. 1980. Tidal clustering and dispersal of
the hermit crab Clibanarius digueti. Mar. Behav. Physiol. 8:
43-53.

SUTHERLAND, J. P. 1970. Dynamics of high and low popu-
lations of the limpet Acmaea scabra (Gould). Ecol. Monogr.
40(1):169-188.

VERNBERG, W. B. & F. J. VERNBERG. 1972. Environmental
physiology of marine animals. Springer-Verlag, Inc.: New
York. 346 pp.

Wara, W. M. & B. B. WRIGHT. 1964. The distribution and
movement of Jegula funebralis in the intertidal region of
Monterey Bay, California. Veliger 6(Suppl.):30-37.

WaARBURG, M. R. 1968. Behavioral adaptations of terrestrial
isopods. Amer. Zool. 8:545-559.

Wo tcotTt, T. G. 1973. Physiological ecology and intertidal
zonation in limpets (Acmaea): a critical look at limiting fac-
tors. Biol. Bull. 145:389-422.

The Veliger 30(2):134-137 (October 1, 1987)

THE VELIGER
© CMS, Inc., 1987

Behavioral Control of Water Loss in the Terrestrial

Slug Deroceras reticulatum (Miller):

Body-Size Constraints

by

THOMAS A. WAITE

Department of Zoology, The Ohio State University, Columbus, Ohio 43210, U.S.A.

Abstract.

I examined the hypothesis that the extent to which the terrestrial slug Deroceras reticulatum

Muller uses behavioral tactics to minimize evaporative water loss is related to body size. Small slugs,
relative to larger individuals, tended to lose more mass (% initial body mass) and tended to spend more
time moving and less time in a contracted posture. However, when moist microhabitats were made
available the correlation between loss in body mass and body size was positive, as small slugs tended
to use these microhabitats more extensively and tended to spend less time moving and more time in a
contracted posture than did larger slugs. The implications of body-size constraints on the water balance

of slugs are discussed.

INTRODUCTION

Terrestrial pulmonate gastropods have moist, highly
permeable integuments that render them vulnerable to
evaporative water loss whenever ambient humidity is lower
than the equilibrium humidity of their blood (approxi-
mately 99.5% r. h. at 20°C; MaAcHIN, 1975). Slugs then
should be able to take in atmospheric moisture only when
relative humidity approaches 100% or when a moist sub-
strate can be contacted so that integumental absorption can
occur (contact-rehydration; MAKRA & Prior, 1985).
However, Cook (1981) reported that, apparently owing
to water loss associated with the production of the mucus
trail for locomotion, specimens of Limax pseudoflavus Ev-
ans continued to lose mass when kept over, but not in
contact with, distilled water for 18 h, even after they had
been dehydrated previously to only 30% of their initial
body mass. This considerable tolerance to dehydration
(DaINTON, 1954; PRIOR et al., 1983), coupled with their
labile haemolymph volume (HUGHES & KERKUT, 1956;
ROACH, 1963), is of obvious adaptive significance for ter-
restrial pulmonates which are often active under desiccat-
ing conditions.

Water-conserving aggregations (huddles) have been ob-
served in the terrestrial slugs Limax pseudoflavus (CHAT-
FIELD, 1976; COOK, 1976; EVANS, 1978), L. maximus (PRI-
oR et al., 1983), and Deroceras reticulatum Muller
(unpublished results). CooK (1981) provided experimental

evidence that (1) the extent and frequency of huddling was
greater in low compared to high humidity conditions, and
(2) slugs that huddled with one other slug experienced a
34% reduction in evaporation rate relative to solitary slugs.
Cook (1981) also demonstrated that L. pseudoflavus re-
sponded to dehydration by moving less frequently and
spending more time in a contracted posture. Huddling
occurs in much the same predictable manner in D. retic-
ulatum (unpublished results). PRIOR et al. (1983) dem-
onstrated that solitary slugs lost more than twice as much
mass as did slugs that had been allowed to huddle.

In this paper I examine a hypothesis concerning effects
of body size on behavioral water-conserving tactics in the
terrestrial slug Deroceras reticulatum Muller. Deroceras re-
ticulatum is a small (generally less than 50 mm in extended
length) nocturnal slug which is native to Europe but has
spread throughout much of North America since its in-
troducticn (BURCH & PATTERSON, 1966; CHICHESTER &
GETZ, 1973). Because small slugs have a greater volume-
specific surface area than larger slugs, their rate of evap-
orative water loss, measured as percent of initial body mass,
should be greater. In fact, in the absence of body-size-
related differences in the behavioral control of water loss,
the rate of evaporative water loss (% initial mass) would
be predicted to vary inversely with initial body mass”.
Therefore, small slugs might be expected to compensate
for their greater vulnerability to dry conditions by (1) more
readily adopting a contracted posture, (2) spending less

T. A. Waite, 1987

Page 135

time moving, and (3) using moist microhabitats with great-
er frequency. These tactics should permit small slugs to
suppress their evaporative water loss below the predicted
rate relative to larger slugs.

MATERIALS anp METHODS

Deroceras reticulatum individuals of various ages were col-
lected at night in Franklin Co., Ohio. They were main-
tained in a terrarium at 26 + 3°C (X + SD) with a 16-h
photoperiod. The slugs were kept on a gravel-loam mixture
that was covered with common dandelion (Taraxacum of-
ficinale) greens. Wheat and barley cereal, rolled oats and
water were provided ad libitum, and apple slices were
provided periodically. The slugs were held from 23 April
to 25 May 1985, and the experiments were conducted
between 1400 and 1900 h at 28°C. Statistical analyses were
performed using Spearman’s rank correlation (SIEGAL,
1956). As this analysis uses ranks, the conversion of initial
body mass (IBM) to IBM” was unnecessary. Statistical
significance was set at the 0.05 level.

I determined the mass of 15 slugs, ranging from 0.057
to 0.944 g, and placed each one in a separate 10 x 1.5-
cm (diameter x height) plastic petri dish. Each petri dish
had, attached to the underside of its lid, a small bag (fash-
ioned from a 5 X 5-cm piece of cheesecloth) containing
anhydrous calcium sulfate. Beginning one min after the
slugs were introduced to the petri dishes, I used a scan
sampling technique (LEHNER, 1979), once each minute for
70 min, and recorded the postural state of each individual
as “moving” (tentacles outstretched, body outstretched, and
moving), “intermediate” (tentacles retracted, body con-
tracted such that the individual’s head was under the an-
terior edge of the mantle flap, and not moving), and “‘con-
tracted” (tentacles retracted, head under the anterior edge
of the mantle flap, and not moving). Immediately following
this 70-min period of observation, I redetermined the mass
of each slug. In order to be able to compute the mean
posture of each individual for the 70 scan samples, I con-
verted each observation of “contracted,” “intermediate,”
and “‘moving” postures to the numeric values of 1, 2, and
3, respectively.

The results of the above experiment (see Figure 1B)
prompted an experiment designed to examine the impor-
tance of microhabitat use with respect to body size. This
experiment tests the prediction that small slugs should
show a greater tendency than should larger individuals to
use moist microhabitats as a means of compensating for
their higher vulnerability to dehydration. The methods
replicate those of the previous experiment with one im-
portant exception. In addition to the desiccant, each petri
dish contained an 8-cm’ porous, water-saturated polysty-
rene cube in which a 2-cm* “tunnel” had been fashioned
on the underside. After determining the mass of 15 slugs,
ranging from 0.150 to 0.914 g, I placed each one in a
separate petri dish. Beginning 1 min thereafter, I recorded
each minute for 60 min (1) the posture of each slug and

PERCENT LOSS
IN BODY MASS

MEAN POSTURE

0 0.2 0.4 0.6 0.8 1.0

INITIAL BODY MASS (g)

Figure 1

Correlations of (A) loss in body mass and (B) mean posture
(where 1 = contracted, 2 = intermediate, and 3 = moving) with
initial body mass of 15 Deroceras reticulatum individuals. P-values
are from two-tailed Spearman’s rank correlation (r,) tests.

(2) whether it was using the microhabitat (defined as mak-
ing contact with either the interior or the exterior of the
polystyrene cube). I then redetermined the mass of each
slug.

RESULTS anp DISCUSSION

Loss in body mass (% of initial mass) (P = 0.0001; Figure
1A) and mean posture (P = 0.0001; Figure 1B) both were
negatively correlated with initial body mass when no moist
microhabitat was available. In other words, small slugs
tended to lose a greater percentage of their initial body
mass and were more active than were large slugs. The
results in Figure 1B contradict the notion that in desic-
cating conditions small slugs (1) should be more likely to
assume a contracted posture, thereby effectively reducing
their evaporative surface area, and (2) should spend less
time moving, an activity that requires the secretion of a
highly aqueous mucus trail. It may be that the small slugs
in this experiment were under such severe body-size con-
straints (namely, their surface-area-to-volume ratios were
prohibitively large) that any water-conserving tactic other
than finding a moist microclimate would have been in-
adequate. That the two smallest individuals died during
this experiment while all others survived lends further
support for this postulation.

In contrast to the above results, when a moist micro-

Page 136

PERCENT LOSS
IN BODY MASS

MEAN PROPORTION
CONTACTING MOIST
MICROHABITAT

MEAN POSTURE

0 0.2 0.4 0.6 0.8 1.0

INITIAL BODY MASS (g)

Figure 2

Correlations of (A) loss in body mass, (B) use of moist micro-
habitat (proportion of observations in which an individual made
contact with the microhabitat) and (C) mean posture (where 1 =
contracted, 2 = intermediate, and 3 = moving) with initial body
mass of 15 Deroceras reticulatum individuals when a moist mi-
crohabitat was available. P-values are from two-tailed Spear-
man’s rank correlation (r,) tests.

habitat was available the correlation between loss in body
mass and initial body mass was significantly positive (P =
0.006; Figure 2A). In addition, small slugs (1) tended to
use the moist microhabitat to a greater extent (P = 0.024;
Figure 2B) and (2) tended to adopt a contracted posture
more frequently and move less often than larger individuals
(P = 0.016; Figure 2C). Thus, when a moist microhabitat
was accessible small slugs behaved as predicted on the basis
of scaling considerations. It appears that the option of using
such a microhabitat aided small slugs in solving their water
loss problem. Admittedly, it could be argued that the moist

The Veliger, Vol. 30, No. 2

microhabitat caused an increase in humidity within the
petri dishes. This criticism, however, fails to account for
the significant positive correlation between loss of body
mass and initial mass; as all 15 individuals lost mass during
the experiment, we still should expect a negative corre-
lation if there were no body-size-related differences in
behavior.

My results prompt the argument that under temporarily
desiccating conditions large slugs have the option of con-
serving water by making postural adjustments. Smaller
individuals exposed to the same conditions for the same
length of time, because of their greater surface-area-to-
volume ratio, should be quicker to reach the point at which
contact-rehydration becomes necessary (60-70% initial body
mass for Limax maximus; PRIOR, 1984). Small slugs thus
should resort quicker than larger individuals to searching
for moist microhabitats. Under such conditions the benefit
of water conservation due to postural adjustments and
reduced mucus production for locomotion presumably
would not outweigh the cost associated with prolonged
exposure for small individuals.

Moreover, my results allow some speculation concerning
how activity budgets of slugs in nature might be related
to body size. One might predict, for instance, that the mean
body size of slugs active under dry conditions would be
skewed upward relative to the mean body size of slugs
active under more humid conditions.

ACKNOWLEDGMENTS

I am grateful to T. C. Grubb, Jr., D. W. Phillips, J. A.
Smallwood, and two anonymous reviewers for their valu-
able comments on an earlier draft of the manuscript. This
study was conducted while I was supported by NSF grant
BSR-8313521 to T. C. Grubb, Jr.

LITERATURE CITED

Burcu, J. B. & C. M. PATTERSON. 1966. Key to the genera
of land gastropods (snails and slugs) of Michigan. Museum
of Zoology, University of Michigan Circular No. 5.

CHATFIELD, J. E. 1976. Limax grossu: Lupu 1970, a slug new
to the British Isles. Jour. Conchol. 29:1-4.

CHICHESTER, L. F. & L. L. Getz. 1973. The terrestrial slugs
of northeastern North America. Sterkiana 51:11-42.

Cook, A. 1976. Trail following in land slugs. Jour. Moll. Stud.
42:298-299.

Cook, A. 1981. Huddling and the control of water loss by the
slug Limax pseudoflavus Evans. Anim. Behav. 29:289-298.

DaINnTON, B. H. 1954. The activity of slugs: I. The induction
of activity by changing temperatures. Jour. Exp. Biol. 31:
165-187.

Evans, N. J. 1978. Limax pseudoflavus Evans: a critical de-
scription and comparison with related species. Ir. Nat. Jour.
19:231-236.

HuGuHEs, G. M. & G. A. KERKuUT. 1956. Electrical activity in
a slug ganglion in relation to the concentration of Locke
solution. Jour. Exp. Biol. 33:282-294.

LEHNER, P. N. 1979. Handbook of ethological methods. Gar-
land STPM Press: New York.

T. A. Waite, 1987

MacHIN, J. 1975. The evaporation of water from Helix aspersa.
I. The nature of the evaporating surface. Jour. Exp. Biol.
41:759-769.

Makra, M.E. & D. J. PRior. 1985. Angiotensin II can initiate
contact rehydration in terrestrial slugs. Jour. Exp. Biol. 119:
385-388.

Prior, D. J. 1984. Analysis of contact-rehydration in terrestrial
gastropods: osmotic control of drinking behavior. Jour. Exp.
Biol. 111:63-74.

Page 137

Prior, D. J..M. HuME, D. VaRGA & S. D. HEss. 1983. Phys-
iological and behavioral aspects of water balance and res-
piratory function in the terrestrial slug, Limax maximus.
Jour. Exp. Biol. 104:111-127.

Roacu, D. K. 1963. Analysis of the haemolymph of Avion ater
L. (Gastropoda: Pulmonata). Jour. Exp. Biol. 40:613-623.

SIEGAL, S. 1956. Nonparametric statistics for the behavioral
sciences. McGraw-Hill: New York.

The Veliger 30(2):138-147 (October 1, 1987)

THE VELIGER
© CMS, Inc., 1987

Responses of a Mussel to Shell-Boring Snails:

Defensive Behavior in Mytilus edulis?

by

THOMAS A. WAYNE

Oregon Institute of Marine Biology, University of Oregon,
Charleston, Oregon 97420, U.S.A.

Abstract.

The mussel Mytilus edulis responded to shell-boring snails of the genus Nucella with valve

gaping, mantle retraction, repetitive valve closures, foot extensions, and changes in byssus attachment
rates. Valve closures frequently pinched snails and occasionally displaced them. Repetitive valve closures
appeared to force snails away from the valve edges. Mytzlus edulis attached more byssal threads to
adjacent Nucella than to adjacent mussels. Attached byssal threads limited snail mobility and sometimes
completely immobilized snails. When the foot of a M. edulis came into contact with Nucella, the snail
tended to move. In addition to moving, snails responded to contact by a M. edulis foot with shell lifting,
shell twisting, and radula strikes. A carnivorous snail that does not bore and two herbivorous snails did
not elicit gaping in M. edulis, nor did another mussel, M. californianus, stimulate shell lifting or shell
twisting by Nucella. Several alternative hypotheses may explain the behavioral responses of M. edulis
to Nucella: (1) the responses are reactions to a paralyzing substance liberated by the snail, (2) they are
shell-cleaning behaviors stimulated by the presence of the snail on the mussel’s valves, and (3) they are
defensive, anti-predator behaviors. The responses of M. edulis to Nucella appear most consistent with
an anti-predator interpretation of their function.

INTRODUCTION

Bivalves are vulnerable to shell-crushing, prying, and
piercing predators such as crabs, seastars, and snails (SEED,
1976). Within the constraints of the bivalve body plan,
which might appear severely to limit behavior, bivalves
have diverse behavioral defenses. ANSELL (1969) docu-
mented the leaping behavior of several clam species which,
when stimulated by seastars, rapidly extend their foot and
lift themselves off the substratum. LAws & Laws (1972)
found that the clam Donacilla responds to a burrowing
gastropod predator by crawling to the surface. Scallops
repeatedly open and close their valves when stimulated by
seastars, thus expelling jets of water sufficient to produce
a type of swimming (FEDER & CHRISTENSEN, 1966).

In contrast to these bivalves, mussels have been thought
to have no such defenses (FEDER, 1972). KIM (1969) ob-
served that the mussel Mytilus edulis exhibited no behavior
other than a prolonged closure of its valves when attacked
by the seastar Asteria amurensis. NIELSON (1975) similarly
observed only prolonged valve closure when M. edulis was
attacked by the predatory gastropod Buccinum undatum.
However, a more recent observation indicates that shell-
boring snails stimulate M. edulis to perform valve move-

ments, prolonged foot-extensions, and attachment of byssal
threads to the snails’ shell. These responses have been
interpreted as defensive behaviors by WAYNE (1980, ab-
stract). MCCONNAUGHEY & ZOTTOLI (1983) similarly in-
terpreted behaviors of M. edulis filmed by Wayne. While
the claim of a behavioral defense in M. edulis has not been
confirmed, such is consistent with bivalve behavior and
ecology.

The purpose of this paper is to describe the previously
identified behaviors of Mytilus edulis (WAYNE, 1980, ab-
stract) and to test for an association between those behav-
iors and stimulation by shell-boring gastropods.

MATERIALS anp METHODS

Preliminary Observations

Experiments were done following several years of pre-
liminary observations, begun in 1976, during which time
the responses of thousands of mussels and hundreds of
snails were viewed. Descriptions and diagrams of behavior
were assembled from observations, photographs, and mo-
tion picture films of mussels and snails interacting in aquaria
under a variety of conditions.

T. A. Wayne, 1987

Experimental mussels and snails were collected at Cape
Arago, the Siuslaw Marina, Pirate’s Cove, and the south
jetties of Coos and Siuslaw bays. These collection sites are
within 80 km of the Oregon Institute of Marine Biology
(Charleston, Oregon), where the observations and exper-
iments were conducted. Running seawater was provided
in all set-ups; seawater temperatures did not exceed ocean
temperatures by more than 2°C. All mussels were Mytilus
edulis Linnaeus, 1758.

Gaping Response of Mussels Exposed in
Aggregate to Free-Moving Snails

A clump consisting of 200-300 Mytzlus edulis was placed
in a 10-gal. (38-L) aquarium. After the mussels attached
byssi and the clump had stabilized, 30-40 snails, Nucella
emarginata (Deshayes, 1839) and N. lamellosa (Gmelin,
1791) (formerly placed in Thazs), were introduced into the
aquarium. A 16-mm Bolex camera with a close-up lens
was used to film the activity on the surface of the clump
at 1 frame per 8 sec. The film was repeatedly viewed at
regular speed in both forward and reverse motions by
projecting the image on a large sheet of paper. The po-
sitions of mussels were drawn on the paper, and the paths
of snails were traced to obtain counts of mussels in each
of two categories: mussels touched by snails and mussels
not touched by snails. For each category, mussels gaping
and mussels not gaping were counted. Mussels were judged
to be gaping when their valves appeared to be open twice
as wide as the valves of adjacent mussels. The results were
entered into a 2 x 2 contingency table and the G-statistic
(SOKAL & ROHLF, 1969) was used to test for independence.

Gaping Response of Mussels Tested Individually

Forty numbered finger bowls (10.5 cm diameter x 4.5
cm) were haphazardly interspersed in a water table. Two
mussels (2-3 cm long) were placed in each finger bowl
and were left undisturbed for 4 h. After this acclimation
period the mussels in 20 of the finger bowls were stimulated
with the smooth tip of a glass rod; the remainder were
stimulated by contact with Nucella emarginata. Stimulation
consisted of light touches to the posterior region of the
mussel’s mantle and valve edges. Each mussel was touched
a total of 15 times at intervals of approximately 1 min
with either the glass rod or a snail. Touches with snails
were accomplished by holding a snail slightly out of water
until it extended its foot; then the extended foot was brought
into contact with a mussel. Mussels gaping and those not
gaping after 15 touches were tabulated for each category
of stimulation. The results were analyzed using the G-sta-
tistic as indicated above.

Byssus Production by Mussels Stimulated
with Nucella emarginata

At the conclusion of the experiment described above,
byssi produced by the glass-rod-stimulated mussels and

Page 139

the snail-stimulated mussels were counted. Mussels pro-
ducing one or fewer byssi were discarded, leaving 29 mus-
sels in each set (one extra mussel was chosen at random
and excluded to make both sets equal). These mussels were
returned to the water table for 12 h, after which time the
byssi were counted again. The production of new byssi in
the two sets of mussels was tested for similarity (one-tailed)
with the Wilcoxon two-sample test (SOKAL & ROHLF,
1969).

Choice Between Mussel and Snail Shell
Substrata for Byssus Attachment

Seventy mussels (2-3 cm long) were placed in individ-
ual, small finger bowls (8 cm diameter x 3 cm) which
were haphazardly distributed in a watertable. Four hours
later, 50 of the most firmly attached mussels were stim-
ulated by Nucella emarginata (stimulation was as previ-
ously described). A plastic grid (1-cm? openings) was placed
over each mussel’s finger bowl; then, one new non-stim-
ulated mussel and one N. emarginata were wedged into
the grid openings. The grid was positioned so that both
the inserted mussel and snail were in comparable prox-
imity to the attached mussel below. Each mussel and snail
inserted into the grid was chosen and placed so as to provide
approximately equal surfaces extending down from the
grid into the finger bowl. These setups were returned to
the watertable where they remained undisturbed for 12 h,
after which time the byssal threads attached to each sub-
stratum choice (the mussel and the snail inserted into the
grid) were counted. Because the mussels had a third choice
of attachment (the finger bowl) that was likely to be se-
lected because of greater area and closer proximity, out-
comes in which mussels failed to attach at least one byssal
thread to a test substratum were excluded in order to
minimize this potentially confounding effect. There were
12 such results. Seventeen more of the original 50 setups
were not acceptable for counting owing to mussel escape,
snail escape, and dislodgment of the grid. The frequencies
of byssal thread attachment to the two substrata were tested
for similarity (one-tailed) with the Wilcoxon two-sample
test.

Specificity of the Gaping Response

Mussels secured to a substratum by byssi may have
different orientations and can move. It is difficult to stim-
ulate such mussels equally or apply consistent criteria for
interpreting their responses. To improve upon this situ-
ation, a method for immobilizing mussels was devised. One
valve was lightly filed to produce a small flat spot, a drop
of cyanoacrylate glue was placed on the flat spot, and the
mussel was held against a plastic slide until firmly at-
tached. The slide was then inserted into a slot (with the
posterior valve edges upright and the valve opening facing
the experimenter) in a specially constructed plastic car-
riage. The mussels remained out of water for 30-60 min
during preparation. The entire carriage with a set of mus-

Page 140

sels (3.0-4.5 cm long) so prepared was lowered into a 5-L
chamber. Control mussels were placed near the chamber’s
seawater inflow (upstream from the experimental mussels)
to avoid stimulating them with water-borne substances that
might emanate from the snails or from the experimental
mussels. Mussels that showed signs of damage or that
failed to open their valves and resume their normal be-
havior during a period of acclimation were discarded.

Gaping was defined to include both a visible increase
in the valve opening and a simultaneous mantle retraction.
Stimulation was carried out as previously described. Each
experiment included a negative control (stimulation by
glass rod) and a positive control. Nucella emarginata was
used as the positive control in the first experiment; in
subsequent experiments, N. lamellosa was used because it
was easier to handle. In addition to testing N. lamellosa in
the first experiment, four other snail species, N. canaliculata
(Duclos, 1832), Searlesia dira (Reeve, 1846), Tegula fu-
nebralis (A. Adams, 1853), and Calliostoma ligatum (Gould,
1849), were tested for their ability to stimulate gaping.
Mussels gaping and those not gaping after 15 stimulations
were tabulated. The data from each experiment were tested
for independence with the G-statistic.

Valve Opening, Mantle Retraction, Valve
Closures, and Foot Extension in Mussels
Stimulated by Nucella emarginata

Mussels used for these experiments were 3.0-4.5 cm
long, and were immobilized on plastic slides and prepared
in amanner similar to that described above. Valve openings
and mantle retractions were measured at the posterior
valve edges using a small section of plastic ruler held with
a long pair of forceps. Mantle retractions to the inside of
the valves were recorded as negative numbers (that is, they
were considered negative extensions). Valve closures were
recorded as observed. Foot extensions and retractions were
voice recorded on an audio tape recorder. The time that a
mussel’s foot remained extended from the valves was then
obtained by review of the tape. After 30-40 min into the
experiment, experimental mussels were intermittently
stimulated for about an hour with Nucella emarginata.
Stimulation was administered as previously described. Data
were recorded before, during, and after the period of stim-
ulation. Another set of mussels prepared in the same man-
ner was used to control for time-dependent variables; these
mussels were not stimulated.

Data were collected in five separate trials, each with
four to six mussels. There were small time differences (10-
30 min) in the pre-stimulation periods among the first few
trials. Valve closures and foot extensions were not recorded
in the first two. Furthermore, some foot-extension data
were lost. All mussels for which both before and after data
were obtained were used in the statistical analysis. Paired
sets of before and after values for valve opening, mantle
retraction, valve closure, and foot extension were tested for

The Veliger, Vol. 30, No. 2

equality in a paired analysis of variance (SOKAL & ROHLF,
1969). The before values were means of measurements
made in the time period before stimulation began. The
after values were means of measurements from an equiv-
alent time period immediately after stimulation ended.

Some of the above data consisted of uninterrupted rec-
ords of sets of valve opening, mantle retraction, valve clo-
sure, and foot extension measured during the pre-stimu-
lation period and continuing until several hours after
stimulation ended. The data in these sets were combined
and plotted to provide a visual illustration of the mussels’
responses.

Shell Lifting and Shell Twisting in
Nucella emarginata

Individuals of Nucella emarginata were filmed at 1 frame
per 4 sec while they were stimulated by contact with a
freshly excised mussel foot; this was followed, after a 5-min
wait, by a second period of stimulation with the foot of a
second mussel species. The mussels used were Mytilus
edulis and M. californianus Conrad, 1837. The order of
stimulation was randomly varied to control for order de-
pendence. The anterior region of the snail’s foot, near the
siphon, was touched repeatedly with a mussel foot for 3
min.

In order to keep the snails in front of the camera, the
snail’s shell was lightly filed and glued (with cyanoacry-
late) to the end of an acrylic rod, which was inserted into
a hole in the top of a 2-L acrylic filming chamber, thus
suspending the snail from the end of the rod into the
seawater below. A small plastic sphere (2.5-cm diameter)
was brought into contact with the snail’s foot, providing a
surface upon which the snail could “move.” Snails in-
variably accepted this surface and began rotating the sphere
with their crawling motions.

Frame-by-frame analysis was done by placing the 16-
mm film over a stage micrometer and viewing the back-
lighted image at x 25. The vertical distance from the lower
edge of a snail’s shell to the lowest part of its foot was
measured directly on the film. The mean of 10 randomly
chosen frames was used to estimate the shell-lifting re-
sponse of each snail. Responses to each type of stimulation
(M. edulis foot vs. M. californianus foot) were tested for
significance in a paired analysis of variance (SOKAL &
ROHLF, 1969).

The maximum horizontal displacement of the snail’s
tissue was also measured directly from the film to obtain
an estimate of shell twisting. Because a twisting snail will
alternately show front and side views (differing in width),
the mean difference in tissue width between successive,
randomly chosen frames (10 frames were chosen at random
and then arranged in ascending order) was used for the
estimate of shell twisting. The responses to the two types
of stimulation were compared in a paired analysis of vari-
ance as indicated above.

T. A. Wayne, 1987

Page 141

Figure 1

Behavioral interactions between the mussel Mytzlus edulis and a shell-boring snail of the genus Nucella. This
sequence (drawn from still photographs and motion picture film) illustrates behaviors that occurred when snails
moved freely among mussels. The dark arrows indicate mussel valve movements; the light arrows indicate snail
shell movements. a. Undisturbed appearance of M. edulis. b and c. Valve opening and mantle retraction following
contact by Nucella. d. Valve closure on Nucella foot. e to h. Mussel foot activity and snail shell lifting and shell
twisting. 1. Byssal threads attached to the snail. j. Snail immobilized by attached byssus. In addition to the events
illustrated here, the snail may be displaced, it may leave its prey, or it may drill and consume the prey.

RESULTS
Preliminary Observations and Descriptions

The interactions between Mytilus edulis and Nucella in-
cluded behaviors that differed in kind and degree from
those observed for mussels or snails alone (Figure 1). Un-
disturbed mussels kept their valves slightly open and ex-
tended their mantle just beyond the valve edges (Figure
1a). Mussels did not react to many organisms that crawled
across their valves, nor did they react when their mantle
was gently touched with a glass rod. They did, however,
retract their mantle and close their valves when strongly
prodded; and, even when undisturbed, they closed their
valves at intervals.

In contrast, mussels gaped widely after contact with
shell-boring snails; the gape was so extreme and the mantle
so strongly retracted that much of the mussels’ internal
anatomy could be seen (Figures 1b, c). Initial contact with
a snail usually produced a momentary valve closure; then,
the valves gradually opened, increasing until an extreme
gape was produced. This condition resembled that of a
dead mussel; yet, gaping mussels reacted to contact and,
once the snails were removed, gradually returned to their
undisturbed appearance.

In addition to gaping, mussels increased their foot ac-
tivity, and they also exhibited intermittent, repetitive valve
closures (the valves closed without any apparent stimulus
and then reopened within seconds) following contact with
shell-boring snails. Snails crawling near a mussel’s valve
edges were sometimes pinched and subsequently moved

away (Figure 1d); some snails fell off when the mussel’s
valves closed.

Unlike the stereotyped patterns of gaping and valve
closures, foot activity was varied and complex. A mussel
might extend its foot over its valves or reach beneath them
as though exploring. Contact with a snail often resulted
in probing and wiping of the snail’s shell and soft tissue
(Figures 1f, g, h). Snails responded to such contact by
moving away, by lifting and twisting their shell (Figures
1f, g, h), or by directing radula strikes toward the mussel’s
foot.

Mussels also attached byssal threads to snails. On oc-
casion, a snail’s twisting motions broke recently attached
threads. The majority of snails placed into aquaria with
large clumps of mussel were eventually immobilized by
byssi or found with broken byssal threads attached to them.
Some snails were found with so many attached threads
that it is doubtful they could have pulled free (Figure 11).
Furthermore, many of the immobilized snails were posi-
tioned with their foot upward (Figure 1j), and appeared
unable to grasp either mussel or substratum.

Gaping Response of Mussels Exposed in
Aggregate to Free-Moving Snails

Ninety-four individual mussels could be seen well enough
on the 16-mm film to be counted (Table 1). Of those that
had been incidentally touched or crawled over by snails
during the filming, 27 were judged to show valve gaping.
Of the mussels that were observed to have no contact with

Page 142

Table 1

Results of two experiments testing for independence of the
gaping response in Mytilus edulis. The results of the first
experiment show counts taken from a film record in which
incidental snail contact was observed and subsequent gap-
ing recorded. The snails were Nucella emarginata and N.
lamellosa. The second experiment compares gaping in mus-
sels individually touched 15 times with either a glass rod
or N. emarginata.

Not

Treatment gaping Gaping G-statistic

Experiment 1

No snail contact 24 0)

Snail contact observed 43 27 ita lertl
Experiment 2

Touch by glass rod 40

Touch by N. emarginata 19 21 Biles eee

eee = P < 0.001.

snails during the filming, none gaped. The probability of
the null hypothesis that gaping in Myézlus edulis is inde-
pendent of contact with the snails (Nucella spp.) is low
(P < 0.001) and the null hypothesis can be rejected.

Gaping Response of Mussels ‘Tested Individually

Stimulating mussels with a glass rod produced no valve
gaping; by comparison, over half the mussels stimulated
with Nucella emarginata gaped (Table 1). Again, the prob-
ability that gaping is independent of the stimulus is low
(P < 0.001).

Byssal Thread Production by Mussels
Stimulated with Nucella emarginata

Mussels initially stimulated by contact with Nucella
emarginata produced fewer byssal threads (5.2 per mussel)
during a subsequent 12-h period than mussels that were
similarly stimulated with the tip of a glass rod (8.1 per
mussel). The two sample distributions differed signifi-
cantly (n = 58, t = 1.86, P < 0.05), and the hypothesis
that byssus production is unaffected by the stimulus can
be rejected.

Choice Between Mussel and Snail Shell
Substrata for Byssus Attachment

Mussels initially stimulated by contact with Nucella
emarginata attached more byssal threads during a subse-
quent 12-h period to live Nucella emarginata (2.8 per mus-
sel) than to live Mytilus edulis (1.3 per mussel). The two
sample distributions differed significantly (n = 42, t =
2.19, P < 0.025) and the hypothesis that mussels will
attach the same number of byssal threads to nearby N.
emarginata as to nearby M. edulis can be rejected. On the

The Veliger, Vol. 30, No. 2

Table 2

Five different gastropods and their effect on gaping in
Mytilus edulis. Touches with a glass rod were used for the
negative control. The positive control was Nucella emar-
ginata in the first experiment and N. lamellosa in the re-
mainder. Stimulation is described in the text.

Not

Treatment gaping Gaping G-statistic

Experiment 1

Negative control 36 0
N. lamellosa 0) 36 IBS Cheer
Positive control 0) 34

Experiment 2
Negative control 24 0
N. canaliculata 0 24 Ol Gere
Positive control 0) 24

Experiment 3
Negative control 19 1
Searlesia dira 19 1 Sila ecerere
Positive control 0) 20

Experiment 4
Negative control 30 0
Tegula funebralis 32 0 1OL.B
Positive control 1 ail

Experiment 5
Negative control 20 0)
Calliostoma ligatum 19 1 SON mamma
Positive control 0 16

PALS SIOZ (ONO,

other hand, at the conclusion of the experiment many
Nucella were found with their foot gripping the experi-
mental mussel. This result changed the original conditions
of the experiment, which provided the experimental mus-
sels with equal proximity to both substrata.

Specificity of the Gaping Response

Each of the five experiments testing different gastropods
for their ability to produce gaping gave highly significant
results (Table 2), in part because of the distinctive contrasts
provided by the positive and negative controls. From a
total of 126 mussels stimulated with the positive control
(Nucella spp.), 125 produced a gape; whereas, only one
mussel was judged to gape out of 130 stimulated with the
negative control (glass rod). Each test of a gastropod’s
ability to produce gaping can be evaluated by inspecting
Table 2 and comparing the snail’s effect with that of the
positive and negative controls.

In the first experiment, the effect of Nucella lamellosa
was the same as the positive control. In the second exper-
iment, the effect of N. canaliculata was the same as the
positive control. In the last three experiments, the effects
of Searlesia dira, Tegula funebralis, and Calliostoma ligatum
were the same as the negative controls.

was Waynes 1987

Valve Opening, Mantle Retraction, Valve
Closure, and Foot Extension in Mussels
Stimulated by Nucella emarginata

Valve opening and mantle retraction were initiated in
Mytilus edulis immediately after contact with Nucella emar-
ginata. When both attributes are plotted on the same graph
(Figure 2A), they provide a distinctive “fingerprint” of the
gaping behavior. The magnitude of the gaping decreased
when stimulation ceased, and it returned to pre-stimulation
values after several hours. Foot extensions were more fre-
quent and prolonged after 30-40 min of stimulation; they
continued long after stimulation ended (Figure 2B). Valve
closures exhibited a similar latent response to stimulation;
they also continued long after stimulation ended (Figure
2C).

Statistical analyses of the complete data set (not the
subset used for illustration and discussed above) show that
before and after values for the experimentals are signifi-
cantly different (Table 3) for valve opening, mantle re-
traction, valve closures, and foot extension time. There
were no significant time-dependent changes in the control
values compared over the same period as the experimentals
(valve opening, n = 11, F = 0.32, P > 0.5; mantle re-
traction, n = 11, F = 1.32, P > 0.25; valve closure, n =
10, F = 1.99, P > 0.10; foot extension, n = 9, F = 0.69,
P > 0.25). Assuming this was also true of the experimen-
tals, the hypothesis that Mytzlus edulis behavior is the same
before and after contact by Nucella emarginata can be re-
jected.

Shell Lifting and Shell Twisting in

Nucella emarginata

Nucella emarginata lifted its shell significantly higher
above the substratum (P < 0.005) when stimulated by a
Mytilus edulis foot than when stimulated by a M. califor-
nianus foot. The mean change in the snail’s horizontal
displacement was also significantly greater (P < 0.025)
when stimulated by a M. edulis foot than when stimulated
by a M. calufornianus foot (Table 4). The hypothesis that
N. emarginata responds similarly to foot contact by M.
edulis and by M. calzfornianus can be rejected.

DISCUSSION

By themselves, the behaviors of Mytilus edulis reported in
this paper are not unusual. Similar results are easily ex-
plained and are probably commonly observed. For ex-
ample, one could expect mussels to attach byssi to snails
by chance alone. Furthermore, both byssus production and
foot activity probably increase while mussels periodically
re-attach themselves to the substratum. Mussels are known
to close their valves in response to chemicals (DAVENPORT,
1977), and they may also close them following physical
disturbance. Some mussels gape on exposure to air (LENT,
1968), and mussels might be expected to gape when in
water with low oxygen. Because bivalves have hinges that

Page 143

exert a tension to open, mussels will also gape as a result
of death, or perhaps injury.

However, such explanations fail to account for the pres-
ent observations. Gaping behavior of Mytilus edulis oc-
curred following contact with the shell-boring gastropods
Nucella emarginata, N. lamellosa, and N. canaliculata. Gap-
ing was not produced by contact with a glass rod, with a
predator that does not bore (Searlesia dira) or with the
herbivorous gastropods Tegula funebralis and Calliostoma
ligatum. Mussels, whether attached by their own byssi or
glued to plastic slides, gaped in response to snails of the
genus Nucella. Although limited in extent, these results
suggest that gaping is a reaction to stimuli associated with
shell-boring gastropods. Additional observations of a pre-
liminary nature indicated that three more shell-boring
snails, Ceratostoma foliatum, Ocenebra interfossa, and O. lur-
ida, stimulated gaping, while additional snails that do not
bore, Oliwella biplicata, Lirularia succincta, and Amphissa
sp., did not. Furthermore, two East coast shell-boring snails,
Nucella lapillus and Urosalpinx cinerea, stimulated gaping
in East coast Mytilus edulis (P. Frank, personal commu-
nication).

Gastropods generally have well-developed chemosen-
sory abilities (CROLL, 1983), and one should expect sessile
prey to respond to such olfactory searching predators by
closing (PALMER et al., 1982). Consequently, the fact the
Mytilus edulis gaped in the presence of Nucella suggests
that the mussel was affected by a toxic or paralytic sub-
stance. A choline ester that slows muscle contraction has
been isolated from the hypobranchial gland of N. emar-
ginata (BENDER et al., 1974). The barnacles Balanus glan-
dula and Chthamalus sp. gape when attacked by Acanthina
punctulata, and the gape has been linked to toxins from
the snail’s hypobranchial gland (SLEDER, 1981). Perhaps
the repetitive valve closures of M. edulis help remove such
substances by increasing water exchange. However, in-
terpreting M. edulis gaping as a reaction to snail toxins is
inconsistent with several other observations suggesting that
gaping mussels are not vulnerable to attack: gaping M.
edults closed their valves when their soft-tissue was touched
by either a snail or a glass rod; gaping mussels increased
their foot activity; Nucella frequently abandoned mussels
that were gaping; and Nucella did not feed on live mussels
through their gaping valves during any of the hundreds of
gapes observed in these experiments, nor are Nucella known
to do so from any reports in the literature. Furthermore,
no gaping was observed in M. calzfornianus during prelim-
inary observations of about 30 individuals stimulated by
Nucella.

The gaping behavior, then, presents a contradiction.
This contradiction could be resolved by one of several
possibilities. First, gaping might be an incidental response
to substances in Nucella that paralyze other prey. Second,
Nucella may induce gaping and then sample mussels to
test their suitability as prey. Third, because choline esters
are known to stimulate escape and avoidance responses
(literature cited by CROLL, 1983), defensive behavior is

Page 144 The Veliger, Vol. 30, No. 2

i0 |] Nucella contact >) Valve Opening :
|

I (0) Experimentals

|
| +
~-O ot + Controls
-O + (e)
2 | Was 9
e 6 |
~ =
as |
oe 4 l
o = 2 =
a Made
S a a,
Ze as ch acne
mie 0 o-2
IP wae Mantle Extension:
rid iNe sit = a? ane e Experimentals
an nd Controls
0 100 200 600
B Time (minutes)
5 8 \Nucella contact oO
= | | Experimentals
= 6 | Controls
ww
= 4
s
ua 2
s yesh)
Medes 0 ahs eas ae
0 100 200 600
C Time (minutes)
4 <I —sNucella contact |
| o Experimentals
EEA Controls
3
=
Ss
oO
S
8
iS
=
=z

Time (minutes)

Figure 2

Temporal changes in the behavior of Mytilus edulis as a function of contact by the shell-boring snail Nucella
emarginata. The values plotted are the means from 6 experimental and 5 control mussels. The vertical bars represent
+1 S.E.; however, note that these data are a subset of those used for significance testing and are themselves not
suitable for such. See text for further information. A. Gaping. The gaping behavior includes valve opening and
mantle retraction (mantle retractions are plotted as negative mantle extensions). The control data are shown as
gray bands to better illustrate the gaping behavior; actual control data points match the pre-stimulation values of
the experimentals. B. Foot activity. Time in minutes that a mussel foot extended outside the valves during each 10-
min period. C. Value movements. Number of valve closures during each 10-min period.

T. A. Wayne, 1987

Page 145

Table 3

Results of paired analyses of variance used to test for

changes in valve opening (nm = 10), mantle extension (n =

10), valve closures (n = 9), and foot extension (n = 8) in

Mytilus edulis following contact with Nucella emarginata.

Means are given for before (pre-stimulation) and after

(post-stimulation) data. See text for method of stimulation
and information on controls.

Mean
Source of ee ea arte AI 0 I
variation Before After df SS F
Valve opening 2.9 mm 6.2 mm
Snail contact iL SOG il Sb
Individuals 9 42.4 1.26
Remainder 93228
Mantle extension 0.3 mm —2.4mm
Snail contact 13328) itor =
Individuals ORES) 0.82
Remainder 9 26.2
Valve closure 0.2 1.2
Snail contact 1 4.49 8.16*
Individuals 8 4.57 1.04
Remainder 8 4.40
Foot extended 0.23 min 1.23 min
Snail contact il BQO OA
Individuals 7 29.8 1638'S
Remainder VT Bei
*= P< 0.025.
SE IP ZS OO,

EA SIP < O05.

suggested. PALMER et al. (1982) suspect that prolonged
withdrawal in Balanus glandula is a chemically mediated
avoidance response. Nucella emarginata is one of the pred-
ators that elicits the response. It is possible that gaping is
an avoidance behavior that obscures information required
by Nucella for prey identification, or perhaps the gape
interferes with the snail’s attack by pushing the snail against
adjacent substrata. However, if gaping is a mussel defense,
then the function of gaping in M. edulis is contrary to what
is found in barnacles, and ability of Nucella to use olfactory
information from M. edulis is contrary to what is expected.

When one considers how mussel valve movements, foot
motions, and byssal thread attachments might affect a shell-
boring snail, it is difficult not to conclude that such be-
haviors increase the snail’s time and energy costs. For
example, from the standpoint of time and energy, the best
place for a snail to drill a mussel is near the valve edges.
Yet, snails seldom drill there. The majority of drill holes
in mussel valves are found in the thicker central region
(CAREFOOT, 1977). In the present study, snails invariably
moved away from the valve edges in apparent reaction to
their movement. Perhaps the valve movement forces snails
into the central region where more time and energy are
required for penetration. Another explanation for the lo-
cation of drill holes in mussels is that the snails may be
attempting to maximize access to the underlying tissues.

Table 4

Shell lifting and shell twisting in Nucella emarginata after

contact by Mytilus edulis and by M. californianus. A paired

analysis of variance was used to test the responses for

similarity (n = 6). See text for method of stimulation and
details of measurement.

Mean response of snail
when stimulated by

Source of M. califor-
variation M. edulis nianus df SS F
Shell lifting 0.74cm ~=0.47 cm
Mussel foot 1 0.33 28.4***
Individuals 5 0.21 3.64
Remainder 5 0.06
Shell twisting 0.22cm 0.05 cm
Mussel foot 1 0.13 10.4*
Individuals 5 0.09 1.5
Remainder 5 0.06
* = P < 0.025.

*** = P < 0.005.

Yet, the snails’ possession of an extensible proboscis would
seem to relax such a strategy. Furthermore, several other
bivalves move their valves in the presence of predators
(CARRIKER & VAN ZANDT, 1972; KIM, 1969) suggesting
a defensive role for valve movement. In addition, STIMSON
(1970) notes that Nucella has a tendency to retract its foot,
lose its grip on the substratum, and be washed away when
pinched by the shell of the owl limpet, Lottia gigantea.
Nucella behaved similarly when pinched by M. edulis valves,
again suggesting that valve movements affect the location
of drill holes. That such pinches dislodged Nucella also
suggests a means by which the sessile mussel may “escape”
its predator.

The foot motions of Mytilus edulis were similar to those
previously described by THEISEN (1972) as shell cleaning
behavior. Shell cleaning involves “licking” motions of the
foot, which remove small particles from the valves. A pos-
sible explanation for the foot activity of M. edulis observed
in the present study is that it was shell cleaning behavior,
and it was stimulated by presence of Nucella on the mussel’s
valves. On the other hand, several aspects of the foot activity
were more suggestive of interference behavior than they
were of shell cleaning. First, the foot was frequently ex-
tended above the valves; thus, “licking” was not the only
behavior observed. Second, several mussels were heavily
encrusted with barnacles; consequently, one should expect
the stimulus for shell cleaning to be obscured. Third, filing
their valves and gluing plastic slides to the mussels did not
stimulate shell cleaning. Fourth, the wiping and probing
motions of the foot appeared to be directed at the snail;
and fifth, the snail frequently moved following contact by
the mussel’s foot.

Mytilus edulis can immobilize Urosalpinx cinerea by at-
taching byssi to the snail’s shell. These immobilizations

Page 146

are not thought to have ecological significance because they
occur at temperatures at which bivalves are active but
snails have gone into hibernation (CARRIKER, 1981). In
the present study, however, M. edulis attached byssi to N.
emarginata and to N. lamellosa at temperatures at which
both mussels and snails were active. As in the case with
U. cinerea, Nucella were often immobilized. These obser-
vations suggest byssal threads are used defensively, inas-
much as byssus attachment to an active snail could, by
restricting the snail’s movement, prolong the attack, cause
the attack to be aborted, or increase the snail’s risk to
predators and physical stress. When provided with two
substratum choices, M. edulis attached more byssal threads
to live Nucella than to live M. edulis, thus indicating that
byssus attachment is biased toward the predator. However,
this result must be interpreted cautiously because the snails
increased their proximity to the mussels during the ex-
periment. On the other hand, such changes in proximity
are an inevitable consequence of a snail’s attack.

The shell-lifting and shell-twisting behaviors of Nucella
could defend it from byssus attachment. Byssal threads
were broken by such motions, and the same motions prob-
ably make byssus attachment more difficult. Similar shell
twisting and shell lifting in other gastropods has been
interpreted as defensive behavior (CLARK, 1958; FEDER,
1967, 1972; PRATT, 1974). Alternately, such behavior in
Nucella might be considered a reaction to food, but this
argument is weakened by the fact that a second, although
not a preferred prey, Mytilus californianus, does not stim-
ulate the same behavior.

CONCLUSIONS

Demographic studies of mussels indicate that they expe-
rience heavy predation in most environments. Some mus-
sels have morphological defenses against predation. Greatly
thickened valves are associated with resistance to shell-
boring gastropods (VERMEIJ, 1978) and such thickened
valves are characteristic of Mytilus californianus. Horse
mussels, Modiolus modiolus, produce tapering hairs or awns
on their periostracum which discourage attachment by the
predatory whelk Thais lapillus (WRIGHT & FRANCIS, 1984).
Predation pressure is especially severe for M. edulis; it is
the preferred prey of at least 10 different invertebrate
predators and is consumed in large numbers by many of
them (SEED, 1969; HARGER, 1972; SUCHANEK, 1978).
Heavy predation by specialized predators should pro-
vide strong selection pressure for the evolution of defensive,
anti-predator mechanisms; however, Mytilus edulis, with
its relatively thin, smooth valves, appears to have poor
morphological defenses against shell-boring snails. On the
other hand, these small, specialized predators stimulate
valve movements, foot motions, and byssus attachment by
M. edulis, all of which could interfere with the snail’s
selection of a drill site and eventual penetration of the
mussel’s valve. Several explanations, including toxic se-
cretions from snails and shell-cleaning behavior, may ac-

The Veliger, Vol. 30, No. 2

count for such responses in M. edulis, but the mussel’s
behaviors appear more consistent with an anti-predator
function. While M. edulis seems to have a poor morpho-
logical defense, the mussel’s responses strongly suggest a
behavioral defense. A comparable situation exists for Teg-
ula aureotincta (SCHMITT, 1981). Like M. edulis, T. aureo-
tincta 1s a preferred prey with an inferior morphological
defense. Significantly, perhaps, 7. aureotincta utilizes a
behavioral defense.

ACKNOWLEDGMENTS

I thank Paul Rudy, Robert Terwilliger, and James Carl-
ton for their help and encouragement. Bayard Mc-
Connaughey and Clifton Gass provided helpful commen-
taries on an earlier version of the manuscript. Peter Frank,
A. R. Palmer, and Johnathan Geller provided additional
suggestions that I have gratefully used in the present ver-
sion. I also thank Lynn Rudy who critiqued the graphs
and diagrams and Kathryn Young who helped with several
experiments and proofread the various drafts. Thanks are
also due Don Rogers for modifying and maintaining lab-
oratory utilities. I am especially grateful to Paul Rudy,
director of the Oregon Institute of Marine Biology, for the
use of laboratory facilities and equipment.

LITERATURE CITED

ANSELL, A. D. 1969. Leaping movements in the Bivalvia. Proc.
Malacol. Soc. Lond. 38:387-399.

BENDER, J. A., K. DERIEMER, T. E. ROBERTS, R. RUSHTON, P.
BooTuH, H. S. Moser & F. A. FUHRMAN. 1974. Choline
esters in the marine gastropods Nucella emarginata and Acan-
thina spirata. Comp. Gen. Pharmacol. 5:191-198.

CAREFOOT, T. H. 1977. Pacific seashores. Univ. Wash. Press:
Seattle. 208 pp.

CARRIKER, M. R. 1981. Shell penetration and feeding by na-
ticacean and muricacean predatory gastropods: a synthesis.
Malacologia 20:403-422.

CaARRIKER, M. R. & D. VAN ZANDT. 1972. Predatory behavior
of a shell-boring muricid gastropod. Pp. 157-244. In: H. F.
Win & B. L. Olla (eds.), Behavior of marine animals. Vol.
I. Plenum Press: New York.

CxiarK, W. C. 1958. Escape responses of herbivorous gastro-
pods when stimulated by carnivorous gastropods. Nature
181:137-138.

CROLL, R. P. 1983. Gastropod chemoreception. Biol. Rev. 58:
293-319.

DAVENPORT, J. 1977. A study of the effects of copper applied
continuously and discontinuously to specimens of Mytilus
edulis exposed to steady and fluctuating salinity levels. Jour.
Mar. Biol. Assoc. U.K. 57(1):63-74.

FEDER, H. M. 1967. Organisms responsive to predatory sea
stars. Sarsia 29:371-394.

FEDER, H.M. 1972. Escape responses in marine invertebrates.
Sci. Amer. 227:92-100.

FEDER, H.M. & A.M. CHRISTENSEN. 1966. Aspects of asteroid
biology. Pp. 87-127. In: R. A. Boolootian (ed.), Physiology
of Echinodermata. Wiley Interscience: New York.

HarGER, J. R. 1972. Competitive co-existence: maintenance
of interacting associations of the sea mussels Mytilus edulis
and Mytilus californianus. Veliger 14:387-410.

AeA Waynes lOSy/

Kim, Y. S. 1969. An observation on the opening of bivalve
mollusks by the starfish, Asteria amurensis. Bull. Fac. Fish.
Hokkaido Univ. 20(2):60-64.

Laws, H. M. & D. F. Laws. 1972. The escape response of
Donacilla angusta Reeve in the presence of a naticid predator.
Veliger 14(3):289-290.

LENT, C. M. 1968. Air gaping by the ribbed mussel, Modiolus
demissus (Dillwyn); effects and adaptive significance. Biol.
Bull. 134:60-73.

McConnNAUGHEY, B. H. & R. ZOTTOLI. 1983. Introduction to
marine biology. Mosby: London. 638 pp.

NIELSEN, C. 1975. Observations on Buccinum undatum L. at-
tacking bivalves and on prey responses with a short review
on attack methods of other prosobranchs. Ophelia 13:87-
108.

PALMER, A. R., J. SZYMANSKA & L. THOMAS. 1982. Prolonged
withdrawal: a possible predator evasion behavior in Balanus
glandula (Crustacea: Cirripedia). Mar. Biol. 67:51-55.

PraTT, D. M. 1974. Behavioral defenses of Crepidula fornicata
against attack by Urosalpinx cinerea. Mar. Biol. 27:47-49.

SCHMITT, R. J. 1981. Contrasting anti-predator defenses of
sympatric marine gastropods (family Trochidae). Jour. Exp.
Mar. Biol. Ecol. 54:251-263.

SEED, R. 1969. The ecology of Mytilus edulis L. (Lamelli-
branchiata) on exposed rocky shores. Part II. Growth and
mortality. Oecologia 3:317-350.

Page 147

SEED, R. 1976. Ecology. Pp. 13-65. Jn: B. L. Bayne (ed.),
Marine mussels: their ecology and physiology. International
Biological Programme 10. Cambridge Univ. Press: Cam-
bridge, London.

SLEDER, J. 1981. Acanthina punctulata (Neogastropoda: Mu-
ricacea): its distribution, activity, diet, and predatory behav-
ior. Veliger 24(2):172-180.

SOKAL, R.R. & F. J. ROHLF. 1969. Biometry. W. H. Freeman:
San Francisco. 776 pp.

STIMSON, J. 1970. Territorial behavior of the owl limpet, Lottia
gigantea. Ecology 51:113-118.

SUCHANEK, T. H. 1978. The ecology of Mytilus edulis L. in
exposed rocky intertidal communities. Jour. Exp. Mar. Biol.
Ecol. 31:105-120.

THEISEN, B. F. 1972. Shell cleaning and deposit feeding in
Mytilus edulis L. (Bivalvia). Ophelia 10:49-55.

VERMEIJ, G. T. 1978. Biogeography and adaptation: patterns
of marine life. Harvard Univ. Press: Cambridge, Massa-
chusetts. 332 pp.

Wayne, T. A. 1980. Antipredator behavior of the mussel Myt-
ilus edulis. Amer. Zool. 20(4):789 (abstract).

WRIGHT, M. M. & L. FRANcIS. 1984. Predator deterence by
flexible shell extensions of the horse mussel Modiolus mo-
dwlus. Veliger 27(2):140-142.

The Veliger 30(2):148-158 (October 1, 1987)

THE VELIGER
© CMS, Inc., 1987

Skeletal Growth Histories of Protothaca staminea

(Conrad) and Protothaca grata (Say) Throughout

Their Geographic Ranges, Northeastern Pacific

by

ROBERT J. HARRINGTON

Department of Geological Sciences, University of California Santa Barbara,
Santa Barbara, California 93106, U.S.A.

Abstract.

The skeletal growth histories of only a few bivalve species have been documented throughout

most or all of their latitudinal ranges. This paper considers growth parameters based on new growth
measurements made throughout the geographic ranges of two bivalve species, Protothaca staminea (Con-
rad) and P. grata (Say). Growth data for a third species, Siliqua patula (Dixon, 1788) by Weymouth
et al. are employed extensively in the study for comparative purposes. The collective range of all three
species extends from the Gulf of Alaska to Panama. The parameters studied include: shell height vs.
age (H,), the rate of decrease in growth rate with ontogeny (defined as the slope of Walford plots and
as e* in the von Bertalanffy growth equation), mean maximum height (H,), and mean maximum
longevity of individuals. Latitudinal trends in the number of daily growth increments formed during
the first full season of growth are contrasted for individuals of both Protothaca species.

All three species exhibit similar growth history trends throughout their respective ranges. Northern
individuals grow slowly but at more uniform rates averaged over ontogeny, and live longer than do
southern phenotypes. High initial growth rates correspond to more rapid decreases in annual growth
rate. The rate of growth deceleration is highly correlated with mean annual sea-surface temperatures.
The number of daily growth increments formed during the first full season of growth is apparently
related to the planetary gradient in sunlight and productivity. The latitudinal rate of change in the

number of daily growth increments is not affected across species boundaries.

INTRODUCTION

Only a few studies have considered skeletal growth pat-
terns over large segments of the latitudinal ranges of mol-
luscan species (e.g., WEYMOUTH et al., 1931; NEWELL,
1964; ANSELL, 1968; GILBERT, 1973; BEUKEMA & MEE-
HAN, 1985), but attempts have not been made to relate
skeletal growth aspects to latitudinal gradients in major
oceanographic factors. Reduced growth rates among higher
latitude phenotypes are expected based on thermodynamic
arguments and the effects of pronounced seasonality in
trophic resource supply. This paper presents evidence that
the effects of temperature and seasonality can be at least
partially distinguished based on analyses of specific skeletal
growth parameters, and that the analysis of skeletal growth
trends can be useful in reconstructing the life histories of
fossil individuals and the states of past oceans.

The research presented is based on growth-history de-

terminations made by the author for two northeastern
Pacific, intertidal, infaunal bivalves, Protothaca staminea
(Conrad) at thirteen localities, and P. grata (Say) at six
localities, throughout most of their composite geographic
ranges from Prince William Sound, Alaska, to Panama
Bay. The growth history of a third congener, P. asperrima
(Sowerby), from a single locality in Panama Bay is in-
cluded. Also included are growth histories of six Pleisto-
cene sample populations of P. staminea representing col-
lections ranging geographically from Bay Center,
Washington, to central Baja California, and a single col-
lection of P. staminea from the Middle to Late Pliocene
Etchegoin Formation of central California. Growth data
provided in WEYMOUTH et al. (1931) based on their study
of latitudinal trends in the growth of Szliqua patula (Dixon,
1788) are included in the analysis for comparative pur-
poses. Geographic trends in growth-history parameters

R. J. Harrington, 1987

documented for Protothaca include annual shell height (H,),
the rate at which growth rate decelerates with ontogeny
(defined as the slope of Walford plots of growth curves
and as e * of the VON BERTALANFFY [1938] growth equa-
tion), maximum mean size (H,), and maximum mean
longevity. Also included are daily growth-increment data
which suggest that their number during the first full season
of growth is closely tied to the planetary gradient in avail-
able sunlight and productivity, and as such may be of value
in the determination of paleolatitudes, and(or) long-term
trends in seasonality at specific latitudes. In all, the growth
histories of more than 500 specimens of Protothaca are
included in the analysis, approximately one-half of these
from the Recent and one-half from the Pleistocene.

Protothaca staminea is the widest ranging and most in-
tensively studied of the congeners (FRASER & SMITH, 1928;
QUAYLE, 1943; SCHMIDT & WARME, 1969; FEDER & PAUL,
1973; PAUL & FEDER, 1973; PAUL et al., 1976; NICKERSON,
1977; FEDER et al., 1979; see also PETERSON, 1977). The
species ranges from Prince William Sound, Alaska, to the
southernmost tip of the Baja California penninsula, but
does not occur in the Gulf of California north of La Paz.
Protothaca grata, one of several tropical to subtropical con-
geners, ranges from the Pacific coast of central Baja Cal-
ifornia where its range overlaps with P. staminea, through
the Gulf of California and as far south as Peru. In the
region of overlap, both species bear striking similarities in
size, shape, coloration, and surface texture. As will be
shown, growth histories of both congeners within their
zone of overlap are sufficiently distinct to separate the
species from one another. The third species, P. asperrima,
ranges from the Gulf of California to Peru but does not
overlap with P. staminea. It is easily distinguished from
the other species of this study by its rasplike, fine surface
texture, but is otherwise closer to P. grata in shell char-
acteristics.

MEASUREMENT anpD SAMPLING
PROCEDURES

Shell heights were measured to the nearest 0.1 mm at
annuli along a curved line from the umbo to the ventral
margin (Figure 1). Specimens were obtained from the
University of California, Los Angeles (UCLA) Depart-
ment of Earth and Space Sciences Museum, the Los An-
geles County Museum of Natural History (LACMNH)
sections of malacology and invertebrate paleontology, and
the University of California, Berkeley Museum of Pa-
leontology (UCMP). Efforts were made to locate specimen
lots that were large and composed of relatively well-pre-
served specimens representative of all size classes. After a
series of preliminary growth-rate determinations were
made, it was determined that large sample sizes were not
necessary to generate representative growth curves for all
localities, and several small lots (less than 10 individuals)
were interposed with larger (25 or more specimens) col-
lections. Collections of fossil specimens were selected fol-

Page 149

Figure 1

Measurement of shell heights at the intersections of annuli with
a curved line from the umbo to the ventral margin.

lowing the same criteria as for the Recent. An additional
criterion was the availability of precise stratigraphic data,
particularly in relation to isotopic stage determinations (see
SHACKLETON & OPpDyYKE, 1976; KENNEDY, 1978).

The preservation of Pleistocene shell material is gen-
erally adequate for the purpose of determining rates of
annual growth. However, the quality of many Pliocene
specimens was too poor to permit accurate direct deter-
minations of growth break positions. In some cases this
problem was overcome by plotting specimens on a Walford
plot (SHELDON, 1965, and see below). In other cases, annuli
weathered out as resistant ridges on the surface of other-
wise poorly preserved specimens, undoubtedly an artifact
of the denser packing of growth increments during the
slow-growth season, and this provided useful data.

SOURCES oF GROWTH-ANNULUS
VARIATION

Several sources of variation in mean annual height vs. age
data can be identified: sample size, the number of individ-
uals surviving to a specific age, geographic dispersion in
the length of the spawning season (and therefore, in con-
ditions experienced when juvenile growth is initiated), car-
ry-over effects of earlier growth increases into later growth
stages, and the latitudinal gradient in the length of the
growing season. Standard deviations in data compiled for
Protothaca staminea throughout its range (HARRINGTON,
1986) indicate that sample size is not a major factor in the
variability of height vs. age. Because survivorship falls with
increasing age, the number of individual data points de-
termining a given age class’s mean size declines, but nor-
mally this does not affect the smoothness of the growth
curve until less than about five specimens represent a given
age class. Standard deviations in height vs. age data do not
measurably increase in Protothaca with ontogeny.
Geographic differences in the duration of the spawning
season and dispersion in the time of settlement have a more
dramatic effect on latitudinal trends in the variance of size

Page 150

60

50

HEIGHT IN MM

1 2 3 4 5 6 7 8

13 9

The Veliger, Vol. 30, No. 2

10 11 #12 13 14 #15 #16 17 #=%18 #19 20

10

AGE IN YEARS
Figure 2

Shell height vs. age curves of 13 Recent collections of Protothaca staminea throughout its range. 1, Whittier, AK;
2, Kayak Is., AK; 3, Dall Is., AK; 4,5, Puget Sound, WA; 6, coastal Oregon; 7, Humbolt, CA; 8, Cayucos, CA;
9, Morro Bay, CA; 10, Long Beach, CA; 11-13, Baja California, Mexico: 11, Estero Punta Banda; 12, Rosarita
Bay; 13, Santa Maria Bay. Note the general increase in the convexity of curves and reduced longevity progressing

from northern to southern localities.

vs. age data. At high latitudes, spawning in Protothaca
staminea is limited to the month of June and standard
deviations in size vs. age data are exceptionally small (FE-
DER et al., 1979; and see NICKERSON, 1977). At lower
latitudes near Victoria, B.C., however, spawning takes
place from April to October (QUAYLE, 1943) and standard
deviations there are substantially greater. KINNE (1972)
has noted progressive increases in the duration of the
spawning season for many temperate invertebrates with
decreasing latitude. CRAIG (1967) observed more scatter
in the position of growth rings in bivalve species sampled
at Bimini lagoon when compared to higher latitude (tem-
perate) species and suggested that this may reflect more
continuous recruitment throughout the year in the Bimini
species. Hence, where spawning is spread throughout more
of the year greater standard deviations in shell heights are
predicted among individuals of a given age.

GROWTH HISTORIES

Growth curves of Recent Protothaca specimens are sum-
marized in Figures 2 and 3. Table 1 contains a listing of
Walford slopes for Protothaca and Siliqua patula through-
out the study region as a function of sea-surface temper-
ature. Walford plots were constructed for each sample in
order to estimate the rate of growth deceleration, maximum

mean size, and maximum longevity of average individuals
(WALFORD, 1946; HANcock, 1965; SHELDON, 1965,
CERRATO, 1980) (Figure 4). Because of the asymptotic
approach of growth curves to a horizontal line, maximum
shell heights must be estimated when employing Walford
plots. In this study, maximum height is taken where 98%
of H,,, (shell height at time t plus one year) has been
obtained by H,. The age that corresponds to this shell
height is taken as the mean maximum longevity of indi-
viduals from the habitat.

Latitudinal Trends in Growth Histories

At the northern range end points of all three species
studied the rate of growth is slower, growth rate deceler-
ation is less pronounced (see below), and longevity is great-
er than at their southern range end points. Maximum sizes
of Protothaca staminea are not observed at extreme high
latitudes, but somewhat south (Table 1). This reflects al-
most negligible height increases during the first few years
of growth for this species in the Gulf of Alaska. In P. grata
and Siliqua patula, initial growth rates are not as markedly
reduced at their northern range end points and the max-
imum sizes are obtained there.

Walford plot slopes represent a quantification of the
rate at which growth decelerates with ontogeny equivalent

R. J. Harrington, 1987

aS
fo}

HEIGHT IN MM

=
fo)

(o)

1 2 3 4 5 6 7 8 9

10

Page 151

11 #12 13 #14 (0) 1 2 3 4 5

AGE IN YEARS
Figure 3

Representative shell height vs. age curves of Protothaca grata (1-4), and P. asperrima (5). 1, Cholla Bay, head of
the Gulf of California; 2, Magdalena Bay, Mexico; 3, Mazatlan, Mexico; 4, Panama Bay; 5, Panama.

to e* in VON BERTALANFFY’s (1938) growth equation.
High Walford slopes represent relatively steady growth
increases from year to year while progressively lower slopes
reflect increasingly pronounced convexity in size vs. age
curves. For Protothaca, slopes decrease from north to south
beginning with a value of 0.91 for P. staminea from Prince
William Sound, Alaska, decreasing to a minimum value
of 0.49 for a sample from Santa Maria Bay (central Baja
California). Protothaca grata specimens also exhibit a max-
imum Walford slope (0.89) at the taxon’s northern range
end point at the head of the Gulf of California, and a
minimum value (0.55) near the southern range end point
of the species at Panama Bay. A Walford plot for the
species P. asperrima from a single locality at Venado Island
in the Canal Zone (near that taxon’s southern range end
point) was constructed yielding a slope of 0.52. Thus, in
the northern hemisphere, Walford slopes on the order of
0.90 typify post-inflection growth of northern range end-
point individuals of Protothaca, while values of 0.50 (or
slightly less) typify the growth of individuals near southern
range end points.

Slopes for Siliqua patula range from a maximum of about
0.70 at the northern range end point in the Gulf of Alaska,
and gradually decrease to a minimum of about 0.33 at the
southern range end point near Pismo, California. Although
these end-point values are less than those of Protothaca, it
is interesting to note that the range of values is approxi-
mately the same (roughly 0.40). The reasons for this dis-
crepancy in range end-point values are not understood. It
is possible that the differences arise from the significantly
more compressed shell geometry of Szlziqua.

Walford slope values for Protothaca staminea, P. grata,
and Siliqua patula are plotted against mean annual sea-
surface temperature estimates taken for each region by
interpolating between 0.5°C surface isotherms determined
for the northeastern Pacific by ROBINSON & BAUER (1976)
(Figure 5). A slightly higher temperature (7.e., 8.6°C. vs.
7.5°C) was taken for Prince William Sound, Alaska, rep-
resenting April through September mean monthly tem-

peratures only (NICKERSON, 1977). This step was taken
so that the temperature estimate was approximately in line
with that actually experienced by Protothaca during its
growth season in the region. Excellent correlations were
obtained with r = —0.938 for P. staminea, r = —0.842 for
P. grata, and r = —0.935 for S. patula, suggesting that
mean annual temperature is a principal environmental
factor determining the slope of the Walford plot, and hence
the rate of annual growth deceleration.

Two samples from Puget Sound yielded seemingly
anomalous slopes of 0.68 and 0.62. As a check for consis-
tency, data from Fraser and Smith (1928) for Protothaca
staminea at Victoria, B.C., yield a value of 0.70. However,
K. Cheu at the University of Washington Department of
Ecology (personal communication, 1985) advises that mean
temperatures within the sound are easily 4°C warmer on
many of the tidal flats than along the Washington outer
coast. This indicates mean annual temperatures for Puget
Sound tidal flats are approximately 12.5°C. Hence, Wal-
ford slopes close to those observed at Cayucos and Morro
Bay, California (e.g., 0.74 and 0.69, respectively) (Table
1) should in fact be expected for the Puget Sound area.

A second latitudinal anomaly in Walford slopes occurs
along northern Baja California, Mexico, where they are
higher than expected for the latitude. As indicated on ocean-
surface temperature maps (ROBINSON & BAUER, 1976),
however, the northern Baja California region is a site of
pronounced coastal upwelling, and mean surface temper-
atures there are nearly identical to the more northern Long
Beach, California locality (Table 1). South of these areas
of upwelling, the decreasing trend in Walford slopes with
latitude may be resumed; the southernmost sample of Pro-
tothaca staminea from central Baja California possesses a
Walford slope (0.49) slightly lower than any of the other
collections. Here temperatures are substantially warmer,
averaging about 17.5°C.

As previously noted, the southernmost range of Proto-
thaca staminea overlaps along the central and southernmost
outer coast of southern Baja California with the north-

Page 152

Table 1

Walford slopes (e*), mean annual sea-surface tempera-
tures, and geographic locations of samples. Temperatures
from ROBINSON & BAUER (1976) except for Alaskan lo-
calities of Protothaca staminea, which are from NICKERSON

(1977).
Water
Wal- tem-
ford _pera-
slope ture
Species (e*) SG: Location
Protothaca staminea 0.91 8.6 Whittier, AK
Protothaca staminea 0.87 8.6 Kayak Island, AK
Protothaca staminea 0.90 8.6 Dall Island, AK
Protothaca staminea 0.68 12.5 Puget Sound, WA
Protothaca staminea 0.62 12.5 Puget Sound, WA
Protothaca staminea 0.83 11.8 Oregon
Protothaca staminea 0.78 12.2 Humbolt, CA
Protothaca staminea 0.74 13.5 Cayucos, CA
Protothaca staminea 0.69 13.5 Mbooro Bay, CA
Protothaca staminea 0.51 16.0 Long Beach, CA
Protothaca staminea 0.59 14.5 Punta Banda, Mex.
Protothaca staminea 0.59 14.5 Rosarita Bay, Mex.
Protothaca staminea 0.49 17.5 S. Maria Bay, Mex.
Protothaca grata 0.89 21.5 Cholla Bay, Mex.
Protothaca grata 0.68 23.0 Guaymas, Mex.
Protothaca grata 0.74 22.0 Magdalena Bay, Mex.
Protothaca grata 0.69 25.5 Mazatlan, Mex.
Protothaca grata 0.63 27.5 Nicaragua
Protothaca grata 0.55 27.3 Panama
Siliqua patula 0.68 6.8 Hallo Bay, AK
Siliqua patula 0.69 6.8 Swickshak, AK
Siliqua patula 0.71 7.2. Karls Bar, AK
Siliqua patula 0.64 9.2 Masset, AK
Siliqua patula 0.48 11.5 Copalis, WA
Siliqua patula 0.54 12.2 Crescent City, CA
Siliqua patula 0.33 13.5 Pismo, CA

ernmost range of P. grata, and the taxonomic separation
of the two species based on gross morphological grounds
is difficult within their zone of range overlap. Growth
histories are useful in distinguishing these species, how-
ever. Two collections from the Magdalena Bay region
exhibit markedly different Walford slopes of 0.49 and 0.74
for P. staminea and P. grata, respectively.

PALEOTEMPERATURE DETERMINATIONS

Growth-history curves are presented for six Pleistocene
and a single Pliocene collection in Figure 6. Slopes were
used to infer paleotemperatures (from Figure 5) and these
were compared with paleotemperature determinations
based on isotopic stage data (see SHACKLETON & OPDYKE,
1976; KENNEDY et al., 1982) (Figure 7) and the distribution
of cold and warm temperature molluscan faunas (KENNEDY,
1978, 1979; KENNEDY e¢ al., 1979, 1982; EMERSON et al.,
1981) for the Pleistocene of the Pacific coast. In general,

The Veliger, Vol. 30, No. 2

paleotemperature estimates based on the regression of
Walford slopes with modern sea temperatures are in good
agreement with data provided from the sources cited above.
The following discussion is organized from the youngest
to the oldest specimen localities.

One of the youngest samples (LACMNH loc. 6913) is
from the 40,000-60,000 year-old, mid-Wisconsin terrace
at Isla Vista (Goleta) near Santa Barbara, California. The
age would place the collection in isotopic stage 3 of SHACK-
LETON & OPDYKE (1976), a period of very cold water even
at this comparatively low latitude. The Walford slope ob-
tained for this sample is 0.84, indicative of a mean annual
temperature on the order of 10.3°C, about 4°C colder than
the mean for this section of the coast today. KENNEDY
(1978) has noted that the faunas at this locality and along
the Santa Barbara and Ventura coastlines contain several
cold-water species presently restricted to the Columbian
Molluscan Province.

Cold water is implied by the growth histories of two
specimens from Cape Blanco, Oregon (UCMP A-8712)
that are of approximately the same age as the cold-water
Isla Vista collection (above). KENNEDY (1978) has noted
a number of species with modern-day Aleutian affinities
at Cape Blanco. Walford slopes suggest slightly colder
paleotemperatures compared to those of Isla Vista. For
Cape Blanco a slope of 0.87 was determined suggesting a
mean annual temperature of about 9.6°C. Although the
slope is based on only two specimens, both exhibited nearly
identical skeletal growth histories.

Two localities, UCLA loc. 4722 from Santa Cruz, Cal-
ifornia, and LACMNH loc. 5662 from Bay Center, Wash-
ington, have been assigned by KENNEDY (1978) to isotopic
stage 5a (SHACKLETON & OPDYKE, 1976), a time of cooler
conditions than occur today. According to Kennedy, Co-
lumbian temperatures may have persisted at least as far
south as central California (e.g., not as far south as during
the colder isotopic stage 3, above); however, the faunal
compositions at Santa Cruz indicate water temperatures
somewhat warmer than expected when compared to the
fauna at Point Ano Nuevo only a few miles north. Kennedy
has attributed this to the coastal physiography of Monterey
Bay, and the lack of upwelling there. J. F. Wehmiiler
(unpublished, in KENNEDY, 1978) notes anomalous warm
air temperatures for the latitude at Santa Cruz occurring
today. The Walford slope for the Santa Cruz collection
indeed reflects warmer than expected paleotemperatures
given the climatic framework of isotopic stage 5a. The
computed slope of 0.60 would suggest an approximate
mean annual paleotemperature of 14.5°C. Based on very
limited data for the Bay Center region, Kennedy suggests
paleotemperatures very close to modern temperatures. The
paleotemperature suggested in the Walford plot of the Bay
Center specimens supports this interpretation; a slope of
0.86 suggests a paleotemperature of about 9.8°C.

Two other Pleistocene localities are approximately
120,000 years old, a time of unusually warm temperatures
(isotopic stage 5e). The first (UCLA loc. 2314) is from

R. J. Harrington, 1987

Page 153

AGE | HEIGHT
1] 102
2 |) 25
E 3 | 29.7
&
= 4 36.2
a 5 | 40.8
ais
(6) | 44.2
(7) | 46.8
(8) | 48.7
(9) | 50.1
10 20 30 40 50 60
H+ (mm)
Figure 4

Construction of a Walford plot from height vs. age data (right). The horizontal axis represents shell height (mm)
at a given age (years). The vertical axis represents shell height one year later. Open circles are values derived from
the growth equation (H,,; = b + mH,), where m is the slope of the Walford plot and b is the intercept with the

vertical axis. H, describes the intersection of the Walford plot line with a line of no growth where H, = H

the Palos Verdes Sand, type locality of the Pleistocene
Verdean Province. Specimens yield a Walford slope of
0.58, indicative of temperatures approaching 15°C. The
second (a composite of UCLA locs. 3447 and 3445) was
taken slightly to the north at the type locality of the Pleis-
tocene Cayucan Province, and indicates a paleotempera-
ture of about 11.2°C based on a Walford slope of 0.79.
The large temperature change over this relatively short
geographic distance during isotopic stage 5e is not sur-
prising. The collections are separated by a major phys-
iographic transition centering today on Point Conception,
and this results in the clustering of sea-surface isotherms
there. If the paleotemperature estimates above are correct,
they suggest the currently steep latitudinal thermal gra-
dient was maintained between the Verdean and Cayucan
Provinces during isotopic stage 5e.

The single Pliocene collection (UCLA loc. 3491) is from
the Etchegoin Formation of Kern County, California. For
these probable Middle to Late Pliocene age specimens,
growth under relatively cool-water conditions is expected
(ADDIcOoTT, 1970). A Walford slope of 0.65 was deter-
mined for a sample of 30 specimens, suggesting a mean
annual temperature of about 13.5°C.

Despite the unknowns concerning the precision of tem-
perature values projected from Walford plots, and the first-
order approximations of temperature based on maps of
sea-surface isotherms, the use of Walford slopes as an
estimate of paleotemperatures appears promising. The ob-

t+1:

vious next step in the research should be to determine
Walford slopes based on a large number of Recent species
throughout their geographic ranges, especially from lo-
cations where mean annual temperatures have been pre-
viously determined. A second future line of research should
be to contrast Walford temperature estimates with deter-
minations based on isotopic compositions of shell material.

LATITUDINAL TRENDS In DAILY
GROWTH-INCREMENT NUMBERS

Criteria employed in the recognition of daily growth in-
crements for Protothaca follow KENNISH (1980) for Mer-
cenaria mercenaria and other references cited in RHOADS
& Lutz (1980). Latitudinal trends in daily growth-in-
crement data (Figure 8) are based on observations in thin-
section, acetate peels, and in polished shells embedded in
resin blocks. The determination of the number of incre-
ments formed within the first growing season is important
because numbers decline with ontogeny. Preliminary evi-
dence suggests that the rate of this decline also varies with
latitude (Figure 9). In some specimens small areas of the
umbonal region were abraded and the number of incre-
ments had to be estimated. This was done by measuring
the distance across the abraded area and then dividing by
the average thickness of adjacent increments. This pro-
cedure should have introduced an error of no greater than
about 10 increments.

Page 154

WALFORD SLOPE

1) 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30

TEMPERATURE °C
Figure 5

Walford slopes plotted against mean annual sea-surface temper-
ature (see text) for Protothaca staminea, P. grata, and Siliqua patula
samples collectively ranging from the Gulf of Alaska to Panama.

The maximum number of daily increments formed dur-
ing the first full growing season increases systematically
with decreasing latitude (Figure 8), and the trend is not
interrupted where congeners overlap. In the Gulf of Alas-
ka, the maximum number of daily growth increments is
about 150, suggesting that Protothaca staminea is meta-
bolically growth-active for only about five months out of
each year. Progressing southward, the numbers of incre-
ments increase gradually such that at Panama Bay, they
number about 331.

The latitudinal trend in increment numbers parallels
the global seasonal pattern of primary productivity in the
world’s oceans (CUSHING, 1959a, b; MENZEL & RYTHER,
1960; RYTHER & MENZEL, 1960; RAYMONT, 1963). A

Pleistocene

HEIGHT IN MM

1 2 3 4 5 6 7 8 9

10

The Veliger, Vol. 30, No. 2

regular trend in the duration and amplitude of primary
productivity undoubtedly affects the length of the growing
season. At high latitudes the season is short and peaked.
Progressing toward the equator, the amplitude of the pro-
ductivity curve flattens substantially, often consists of two
modes at mid-latitudes, and very near the equator is ex-
tremely low, but of much greater duration. The global
distribution of available sunlight is considered of principal
importance in the initiation of annual productivity, where-
as the role of temperature is relatively minor. This being
the case, then it should be expected that the regular trend
in daily increment numbers vs. latitude (Figure 8) should
more closely reflect trophic resource seasonality patterns
than temperature effects.

DISCUSSION

Several factors structure the growth histories of post-larval
individuals throughout the northeastern Pacific range of
Protothaca. Two of the most important factors are the range
of temperatures experienced by individuals, and the sea-
sonal pattern of primary productivity. Other factors such
as salinity and water chemistry are considered to contribute
a relatively insignificant effect on growth-history differ-
ences over the broad geographic scale evaluated in the
study.

Temperature is known to determine the rate at which
food may be metabolized, and hence, should substantially
affect the seasonal pattern of increasing and decreasing
daily increment thicknesses. Such trends have been well
documented for a number of bivalve taxa (e.g., PANNELLA
& MAacC.Lintock, 1968; RHOADS & PANNELLA, 1970;
ARTHUR et al., 1983). The effect of seasonal patterns in
trophic resource abundance on the thicknesses of daily
growth increments, and questions involving the energetics
of calcium carbonate precipitation over the range of tem-
peratures that bivalve species experience, remain as im-
portant areas of future research.

Pliocene

Aa N20 ASE AY 15) ATO A 2) ar aT rs) 6)

AGE IN YEARS
Figure 6

Pleistocene (1-6) and Pliocene (7) shell height vs. age curves of Protothaca staminea. 1, Isla Vista, CA; 2, Cape
Blanco, OR; 3, Santa Cruz, CA; 4, Bay Center, WA; 5, Palos Verdes, CA; 6, Cayucos, CA; 7, Etchegoin Fm.,

central CA.

R. J. Harrington, 1987

ka O 100 200 300 400

Page 155

MATUYAMA

500 600 700

Figure 7

Isotopic stages redrawn from SHACKLETON & OPDYKE (1976). Peaks represent relatively warmer paleotemperatures.

The seasonal pattern of trophic resource supply is clear-
ly important in determining the length of the growing
season at different latitudes and this is apparently best
recorded in the number of growth increments formed dur-
ing the first full season of growth experienced by individ-
uals. However, as shown earlier (Figure 9) the number
of increments recorded within annual growth bands de-
creases systematically with increasing age. One explana-
tion for this decline could be that ever-increasing energy
is expended each year in other metabolic activities such as
reproduction and maintenance. It has yet to be determined,
however, if fewer days are recorded at the beginning of
the growth season, at the end, or if the pattern of growth
increment formation is simply more intermittent through-
out the year. This hypothesis could be tested by contrasting
some measure of the seasonal pattern of reproductive effort
against growth expenditures for a series of age classes.

Near the southern range end point of a species, the
growing season is relatively longer, and temperatures
warmer on the average, than along more northern segments
of its range. The combination of these factors acts to max-
imize the initial annual growth rate of Protothaca. Whether
the higher rate of growth deceleration and reduced lon-
gevity at lower latitudes are consequences of initial (per-
haps wasteful) growth expenditures as has been suggested
by WEYMOUTH et al. (1931), or whether they result from
the relaxation of selection for continued size increases after
a minimum adaptive size is obtained, is unclear. Trans-
plantation experiments (e.g., SEED, 1968) that document
rejuvenated growth late in life argue against models based
on pre-determined lifetime metabolic allocations.

One explanation arises if the relatively reduced rate of
ontogenetic growth deceleration (and increased longevity)
is viewed from the standpoint of potential lifetime repro-
ductive commitments. For example, if high latitude phe-
notypes followed a similar schedule of growth rate decline
as their low latitude counterparts, their size and potential
reproductive contributions at any given age would be vol-
umetrically reduced (Harrington, in preparation). Hence,
high-latitude individuals may rely on a strategy that acts,
perhaps through allelic substitutions, to maximize the du-
ration of growth activity each season, and perhaps to in-

crease longevity. Table 2 contrasts predicted total lifetime
reproductive contributions for individuals near the range
end points and range midpoint of Protothaca staminea, as-
suming that fecundity is uniformly a 50% function of soft-
tissue volume. Although this tabulation represents only
gross estimates of lifetime reproductive effort, it is signif-
icant in two respects. First, the reproductive contributions
for individuals located near the respective range end points
are nearly identical. This suggests that range end points
may not be determined by thermal effects per se (z.e., heat
or cold death) but by population recruitment effects stem-
ming from (temperature and seasonality-dependent)
growth-history patterns. Secondly, individual reproductive
contributions and potential population recruitment levels
are maximized near the range midpoint of the species.
Thus, it should be expected that population sizes are great-
est and perhaps most stable there (see BROWN, 1984).
Viewed from the standpoint of relative life-history strat-
egies (STEARNS, 1976), it is apparent that northern range
end-point representatives, in effect, hedge their reproduc-
tive bets by virtue of delayed contributions (due to slower

Daily Increment Number

10 20 30 40 50 60 70

Latitude

e
(Equator)

Figure 8

The number of daily growth increments formed during the first
full season of growth (see text) based on single specimens of
Protothaca from the Gulf of Alaska to Panama.

Page 156

aS
(2)
[o)

wo
[o)
[o)

200

100

NUMBER OF DAILY GROWTH INCREMENTS

The Veliger, Vol. 30, No. 2

O Callista chione
N. Adriatic Sea (45°N)

® Protothaca staminea
Prince Willlam Sound, Alaska

9 10 1
AGE

Some Neal cane LEE Te aU
i W218 14 1 We Ir 18

Figure 9

Ontogenetic decrease in the number of daily growth increments for a specimen of Protothaca staminea from the Gulf
of Alaska (lower curve) and Callista chione (upper curve) from the northern Adriatic Sea. Data for C. chione are
extracted from HALL (1975) by combining the number of growth increments in the “fast growth band” and the
“biocheck” at given ages from Hall’s curve (HALL, 1975:fig. 4). Note that the rate of decrease is greater for C.

chione.

growth) and significantly greater longevity. Meanwhile,
southern phenotypes can be viewed as relative r-strategists;
reproductive contributions are maximized among relative-
ly young individuals. For example, by age 4 the southern
phenotypes have produced as many potential offspring per
capita as do northern phenotypes by age 12 (Table 2). In
terms of actual population recruitment potentials for Pro-
tothaca staminea this analysis awaits data based on lati-
tudinal differences in survivorship. For Siliqua patula,
however, the general pattern is of progressively lower age-
specific mortality at higher latitudes (WEYMOUTH et al.,
1931). If this survivorship trend also applies to Protothaca,
then smaller age-specific reproductive efforts among young,
northern individuals should be at least partially overcome
by the more significant reproductive contributions of rel-
atively larger, older age classes.

The employment of growth-history patterns may pro-
vide useful data to a variety of paleontological problems.
Potential paleotemperature applications have been sug-
gested in a previous section. As a paleobiogeographic tool
the patterns observed suggest a means by which the geo-
graphic position of a fossil sample with respect to its species
range end points might be suggested. For example, Wal-
ford slopes of approximately 0.90 should indicate prox-
imity to northern, and values of approximately 0.50 to
southern range end-point positions.

Latitudinal trends in the number of daily growth in-
crements formed during the first full season of growth may

Table 2

Estimated age-specific shell volumes for individuals of Pro-

tothaca staminea from northernmost, mid-range, and south-

ernmost localities. Total reproduction is taken as one-half

of the sum of shell volumes at age. Volumes derived from
curve in HARRINGTON (1986).

Gulf of Alaska Cayucos, CA Baja California

Age Height Volume Height Volume Height Volume

(yr) (mm) (mL) (mm) (mL) (mm) (mL)
1 2.69 <1.0 10.23 1.2 14.90 1.8
D, 5.76 <1.0 21.54 Dell 27.10 4.3
3 8.93 1.0 29.70 6.0 34.30 9.0
4 12.63 15 36.20 10.5 38.53 12.8
5 15.68 1.9 40.76 16.0 41.04 16.4
6 18.20 Dob 44.13 20.0 42.51 18.2
7 20.58 D5 46.73 24.2 — —
8 22.82 2.9 48.66 27.8 — —
9 24.50 3.5 50.10 30.7 — —
10 26.10 3.9 51.18 31.5 — —
11 27.49 4.4 51.97 33.0 — —
12 28.71 5.1 = — —_ —
13 29.78 6.0 — — — —_
14 30.70 6.5 = — —_— —_—
15 Sil Sil 7.0 = — — —
16 32.22 _ 71.5) — = = =
Total volume 58.0 175.8 62.5
Total produc-
tion 29.0 87.9 Sil 2

R. J. Harrington, 1987

provide information useful in documenting latitudinal
translations of crustal blocks. Because high-latitude phe-
notypes should typically record a low number of incre-
ments, shells from high-latitude fossil deposits bearing
anomalously high increment numbers in the first annulus
should signal that large-scale latitudinal translations may
have occurred. However, much more data are needed in
order to determine the generality of the association between
increment numbers and latitude. In addition, increment
numbers may be useful in the evaluation of finer-scale
trends in seasonality over given latitudinal regions.

As a potential tool in the correlation of rock units, growth-
history analysis may lead to more precise local correlations
reflecting localized temperature effects. Refined strati-
graphic subdivisions of fossiliferous rock units may be
based on at least three growth-history criteria: (1) the rate
of growth deceleration, (2) initial annual growth rates, and
(3) the thickness of growth increments and their rate of
decline in numbers during ontogeny.

ACKNOWLEDGMENTS

My grateful appreciation is extended to J. W. Valentine,
S. M. Awramik, and J. A. Mattinson of the Department
of Geological Sciences, University of California, Santa
Barbara, who served on the author’s dissertation commit-
tee. A. Clarke, British Antarctic Survey, P. W. Frank,
University of Oregon, G. L. Kennedy, Los Angeles County
Museum of Natural History, J. W. Valentine, and an
anonymous reviewer each contributed many constructive
criticisms of earlier versions of the manuscript.

Partial financial support was obtained through the Uni-
versity of California Institute of Marine Resources, a Geo-
logical Society of America Research Grant, the National
Science Foundation NSF-EAR 17011, and the Depart-
ment of Geological Sciences, University of California, San-
ta Barbara. Mary Parrish, United States Museum of Nat-
ural History, provided assistance in drafting the figures,
and Lorie Harrington provided substantial support in the
preparation of the original manuscript.

LITERATURE CITED

AppicoTT, W. C. 1970. Latitudinal gradients in the Tertiary
molluscan faunas of the Pacific coast. Palaeogeog., Palaeo-
climatol., Palaeoecol. 8:287-312.

ANSELL, A. D. 1968. The rate of growth of the hard clam
Mercenaria mercenaria (L.) throughout the geographic range.
Jour. Cons. Perm. Int. Explor. Mer 31:364-409.

ARTHUR, M. A., D. F. WILLIAMS & D. S. JONEs. 1983. Sea-
sonal temperature-salinity changes and thermocline devel-
opment in the mid-Atlantic Bight as recorded by the isotopic
composition of bivalves. Geology 11:655-659.

BEUKEMA, J. J. & B. W. MEEHAN. 1985. Latitudinal variation
in linear growth and other shell characteristics of Macoma
balthica. Mar. Biol. 90:27-34.

Brown, J. H. 1984. On the relationship between abundance
and distribution of species. Amer. Natur. 124:255-279.
CERRATO, R. M. 1980. Demographic analysis of bivalve pop-

ulations. Pp. 417-465. In: D. C. Rhoads & R. H. Lutz

Page 157

(eds.), Skeletal growth of aquatic organisms. Plenum: New
York.

Craic, G. Y. 1967. Size-frequency distributions of living and
dead pelecypods from Bimini, Bahamas, B.W.I. Jour. Geol.
75:34-45.

CusHING, D. H. 1959a. On the nature of production in the
sea. Fish. Invest. Lond. Series II. 22:1-40.

CusHING, D. H. 1959b. The seasonal variation in oceanic pro-
ductivity as a problem in population dynamics. Jour. Cons.
Perm. Int. Explor. Mer 24:455-464.

EMERSON, W. K., G. L. KENNEDY, J. F. WEHMILLER & E.
KEENNAN. 1981. Age relations and zoogeographic impli-
cations of Late Pleistocene marine invertebrate faunas from
Turtle Bay, Baja California Sur, Mexico. Nautilus 95:105-
116.

FEDER, H. M. & A. J. PAUL. 1973. Abundance estimates and
growth rate comparisons for the clam Protothaca staminea
from three beaches in Prince William Sound, Alaska with
additional comments on size-weight relationships, harvesting
and marketing. Univ. Alaska Inst. Mar. Sci. Tech. Report
No. R73-3:34 pp.

FEDER, H. M., J. C. HENDEE, P. HOLMEs, G. J. MUELLAR &
A. J. PauL. 1979. Examination of a reproductive cycle of
Protothaca staminea using histology, wet-dry weight ratios,
and condition indices. Veliger 22:182-187.

FRASER, C. M. & G. M. SMITH. 1928. Notes on the ecology
of the littleneck clam, Paphia staminea Conrad. Trans. Roy.
Soc. Can. Ser. 3, 22, Sect. V:249-269.

GILBERT, M. A. 1973. Growth rate, longevity and maximum
size of Macoma balthica (L.). Biol. Bull. 145:119-126.
HALL, C. A., JR. 1975. Latitudinal variation in shell growth
patterns in bivalve molluscs: implications and problems. Pp.
163-175. In: G. D. Rosenberg & S. K. Runcorn (eds.),
Growth rhythms and the history of the earth’s rotation. John

Wiley and Sons: London.

Hancock, D. A. 1965. Graphical estimation of growth pa-
rameters. Jour. Cons. Perm. Int. Explor. Mer. 29:340-351.

HARRINGTON, R. J. 1986. Growth patterns within the genus
Protothaca (Bivalvia: Veneridae) from the Gulf of Alaska to
Panama: paleotemperatures, paleobiogeography, and paleo-
latitudes. Doctoral Thesis, University of California, Santa
Barbara. 235 pp.

KENNEDY, G. L. 1978. Pleistocene paleoecology, zoogeography
and geochronology of marine invertebrate faunas of the Pa-
cific Northwest coast (San Francisco Bay to Puget Sound).
Doctoral Thesis, University of California, Davis. 824 pp.

KENNEDY, G. L. 1979. Pleistocene marine faunal provinces of
California. Appendix to K. R. LaJoie, J. P. Kern, J. F.
Wehmiller, S. A. Mathieson, A. M. Sarna-Wojcicki, R. F.
Yerkes & P. A. McCrory (1979), Quaternary marine shore-
lines and crustal deformation, San Diego to Santa Barbara,
California. Pp. 3-15. Jn: P. L. Abbott (ed.), Geological ex-
cursions in the southern California area (Dept. Geol. Sci.,
San Diego State Univ., San Diego).

KENNEDY, G. L., K. R. LAJOIE & J. F. WEHMILLER. 1979.
Late Pleistocene and Holocene zoogeography, Pacific north-
west coast. Geol. Soc. Amer. Abstr. Prog. 11:87.

KENNEDY, G. L., K. R. LAJOI & J. F. WEHMILLER. 1982.
Aminostratigraphy and faunal correlations of late Quater-
nary marine terraces, Pacific coast, USA. Nature 299:545-
547.

KENNISH, M. J. 1980. Shell microgrowth analysis: Mercenaria
mercenaria aS a type example for research in population
dynamics. Pp. 255-294. In: D. C. Rhoads & R. A. Lutz
(eds.), Skeletal growth of aquatic organisms. Plenum: New
York.

Page 158

KINNE, O. 1972. Temperature. Pp. 321-616. In: O. Kinne
(ed.), Marine ecology Vol. 1. Wiley Interscience: London.

MENZEL, D. W. & J. H. RYTHER. 1960. The annual cycle of
primary production in the Sargasso Sea, Bermuda. Deep Sea
Res. 6:351-367.

NEWELL, N. D. 1964. Physiological aspects of the ecology on
intertidal molluscs. Pp. 59-81. In: R. M. Wilbur & C. M.
Yonge (eds.), Physiology of Mollusca. Vol. 1. Academic Press:
London.

NICKERSON, R. B. 1977. A study of the littleneck clam (Pro-
tothaca staminea Conrad) and the butter clam (Saxzdomus
giganteus Deshayes) in a habitat permitting coexistence, Prince
William Sound, Alaska. Proc. Natl. Shellfish Assoc. 67:85-
102.

PANNELLA, G. 1975. Paleontological clocks and the history of
the earth’s rotation. Pp. 253-284. In: G. D. Rosenberg &
S. K. Runcorn (eds.), Growth rhythms and the history of
the earth’s rotation. John Wiley and Sons: London.

PANNELLA, G. & MACCLINTOCK. 1968. Biological and envi-
ronmental rhythms reflected in molluscan shell growth. Jour.
Paleontol. 42:64-80.

PauL, A. J. & H. M. FEDER. 1973. Growth recruitment and
distribution of the littleneck clam, Protothaca staminea in
Galena Bay, Prince William Sound, Alaska. Fish Bull. 7:
665-677.

PauL, A. J., J. M. Pau & H. M. FEDER. 1976. Recruitment
and growth in the bivalve Protothaca staminea at Olson Bay,
Prince William Sound ten years after the 1964 earthquake.
Veliger 18:385-392.

PETERSON, C. H. 1977. Competitive organization of the soft-
bottom macrobenthic communities of southern California
lagoons. Mar. Biol. 43:343-359.

QuaAYLE, P. B. 1943. Sex, gonad development and seasonal
gonad changes in Paphia staminea (Conrad). Jour. Fish. Res.
Bd. Canada 6:140-151.

The Veliger, Vol. 30, No. 2

RayMonrtT, J. E. G. 1963. Plankton and Productivity in the
Oceans. Pergamon Press: New York. 660 pp.

Ruoapbs, D. C. & R. H. Lurz (eds.). 1980. Skeletal growth
of aquatic organisms. Plenum: New York. 750 pp.

Ruoaps, D. C. & G. PANNELLA. 1970. The use of molluscan
shell growth patterns in ecology and paleoecology. Lethaia
3:143-161.

RoBINnsoNn, M. K. & R. A. BAUER. 1976. Atlas of North Pacific
Ocean monthly mean temperatures and mean salinities of
the surface layer. Naval Oceanographic Office, Washington,
D.C.

RYTHER, J. H. & D. W. MENZEL. 1960. The seasonal and
geographic range of primary production in the Western Sar-
gasso Sea. Deep Sea Res. 6:235-238.

SCHMIDT, R. R. & J. E. WARME. 1969. Population charac-
teristics of Protothaca staminea (Conrad) from Mugu Lagoon.
Veliger 12:193-199.

SEED, R. 1968. Factors influencing shell shape in Mytilus edulis
L. Jour. Mar. Biol. Assoc. U.K. 48:561-584.

SHACKLETON, N. J. & N. D. OPDYKE. 1976. Oxygen isotope
and paleomagnetic stratigraphy of Pacific core V28-239, late
Miocene to latest Pleistocene. Geol. Soc. Amer. Mem. 145:
449-464.

SHELDON, R. W. 1965. Fossil communities with multi-modal
size-frequency distributions. Nature 206:1336-1338.

STEARNS, S.C. 1976. Life-history tactics: a review of the ideas.
Quart. Rev. Biol. 51:3-47.

VON BERTALANFFY, L. 1938. A quantitative theory of organic
growth (Inquiries on growth laws II). Human Biol. 10:181-
AD

WALFORD, L. A. 1946. A new graphic method of describing
the growth of animals. Biol. Bull. 90:141-147.

WEYMOUTH, F. W., J. C. MCMILLIN & W. H. RicH. 1931.
Latitude and relative growth in the razor clam Siliqua patula.
Jour. Exp. Biol. 8:228-249.

THE VELIGER
© CMS, Inc., 1987

The Veliger 30(2):159-166 (October 1, 1987)

Age and Growth of the Subantarctic Limpet
Nacella (Patinigera) magellanica magellanica
(Gmelin, 1791) from the Strait of Magellan, Chile
by

LEONARDO F. GUZMAN anD CARLOS F. RIOS

Instituto de la Patagonia, Universidad de Magallanes,
Casilla 113-D, Punta Arenas, Chile

Abstract. Age and growth rate of the subantarctic limpet Nacella (Patinigera) magellanica magellanica
(Gmelin, 1791) from intertidal cobble-boulder fields of the Strait of Magellan were determined. Growth
was defined using exterior shell growth lines and employing the Ford-Walford relationship and von
Bertalanffy model. Males and females did not show significant differences in growth and, according to
estimated growth parameters, which varied geographically along the Strait, the ten studied populations
can be segregated into four distinct groups. A seasonal growth pattern, with higher growth rates during
spring-summer and lower rates during autumn-winter, was present which correlates with seasonal
fluctuations of physical and biological conditions of the Strait. Initiation of annulus formation might
occur between the end of summer and the beginning of autumn. A low annual growth rate (K = 0.0263 —
0.1913), a low instantaneous rate of natural mortality (M = 0.026 — 0.191), and a long life (15.7-
37.8 yr) were characteristics of the studied populations. Growth rate and longevity were inversely
correlated. The western populations of the studied area had the highest growth rates and the lowest
longevities, while the eastern populations showed the opposite trend. The observed growth pattern was
inversely correlated with tidal range, but this single physical factor alone did not explain the trend.

INTRODUCTION

Comprehensive studies on growth and age have been un-
dertaken for many marine gastropods at different latitudes
(FRANK, 1969; BRANCH, 1974; BRETOS, 1980; COCKCROFT
& FORBES, 1981), including the Antarctic region (PICKEN,
1979, 1980). However, comparatively little information
exists for gastropods inhabiting the subantarctic zone (e.g.,
BLANKLEY & BRANCH, 1985).

Among the subantarctic gastropods, the Nacella (Pati-
nigera) complex is well represented within southern Pat-
agonia and Tierra del Fuego of Chile and Argentina (z.e.,
the Magellanic molluscan province; POWELL, 1973). Pow-
ell considers this complex to be constituted by cold water
limpets with the greater part of their range being subant-
arctic. Nacella (Patinigera) magellanica magellanica (Gme-
lin, 1791) is one of the 14 species of the genus Nacella
Schumaker, 1928, recognized in the subantarctic zone, and
one of the most common inhabitants of the beaches of
Tierra del Fuego, the Strait of Magellan, and the Falk-
lands Islands (POWELL, 1973).

Biological information for this species is scarce, although
its geographical and bathymetric distributions (CARCELLES
& WILLIAMSON, 1951), diagnostic features (DELL, 1971;
POWELL, 1973; OTAEGUI, 1974), density, and spatial pat-
tern of distribution (GUZMAN, 1978) have been studied.
The aim of the present study was to determine age and
growth for 10 intertidal populations of Nacella (P.) ma-
gellanica and to provide baseline data from which predic-
tions and comparisons could be made.

MATERIALS anp METHODS

Samples of Nacella (P.) magellanica were obtained from
10 sites located in the Strait of Magellan, from the second
narrow to its eastern entrance (Figure 1). Except for Punta
Catalina, where the physical habitat is characterized by a
hard clay terrace, the other sites are typical cobble-boulder
beaches. The sites have a wide range of sediment sizes,
exposures to wave action, slopes, and tidal amplitudes (see
GUZMAN, 1978).

Fifty limpets at each site were randomly collected from

Page 160

The Veliger, Vol. 30, No. 2

52°30!

53°00!

L\

Bahia San Gregorio
Bahia Santiago
Punta Delgada
Punta Tandy

Bahia Posesion
Punta Wreck

Punta Remo

Punta Baxa

Punta Espora

= Punta Catalina

AMDaevIAOYNo
tu

Figure 1

Location of the study area including sampling sites in the Strait of Magellan.

the mid-intertidal zone during spring 1977, winter 1978,
and summer 1978 and 1979. Specimens from Punta Tandy
were sampled in fall and spring 1980. In the laboratory
the specimens were sexed by direct observation of the go-
nads, and the shell was used for growth measurements.

Growth was estimated by the growth ring method, which
requires the establishment of rings as annual marks on
the shell of the species under study (WILBUR & OWEN,
1964). This approach has been employed successfully in
growth and age estimations in patellid (PICKEN, 1980),
fissurellid (BRETOS, 1980, 1982), trochid (WILLIAMSON &
KENDALL, 1981), and muricid (MIRANDA, 1975) species.

On the exterior shell surface of Nacella (P.) magellanica
growth marks are present. It was assumed that the marks
correspond perfectly to true annuli and, consequently, they
were used for aging purposes (see Discussion). The max-
imum length of each consecutive growth ring from the
front of the ring to its posterior margin was measured to
the nearest 0.1 mm with vernier calipers. Separate infor-
mation for females, males, and sexually undetermined
specimens was recorded.

Measurements of consecutive rings were not assigned
to specific ages owing to difficulties in assessing the rings
on the shell apex, which is usually eroded. Thus, growth
was inferred by plotting the correspondent pairs of con-
secutive ring lengths measured in each specimen, grouped
by sampling periods and by sexes, according to the Ford-
Walford method (WALFORD, 1946). This method basically
consists of the linear relation of size at t years against size
at t + 1 years.

Age was inferred from VON BERTALANFFY’s (1938)
growth model. The parameters K (growth coefficient) and
L.. (asymptotic length) were derived from the regression
coefficients of the Ford-Walford plots, while the theoretical
age at length zero (t,) was computed following GULLAND

(1965). The age at which 95% (p) of the asymptotic length
or theoretical age limit (A,) was reached, the instantaneous
rate of natural mortality (M), and the fraction of an initial
stock that would die during a year or conditional mortality
rate (A) were derived from t, and K parameters following
TAYLOR (1959). In this study, M is equivalent to the total
instantaneous mortality rate (Z).

In order to evaluate both annual ring formation and
seasonality in growth, the yearly marginal shell increment
at six sites was evaluated. For this purpose, 10 shells from
winter, spring, and summer samples were randomly cho-
sen within an age range (7-9 yr) defined by the corre-
spondent growth equation. Marginal increments were de-
termined on the posterior edge of the shell, by measuring
the distance from the last distinguishable growth ring to
the edge of the shell using a stereomicroscope (16) with
a precision of +0.02 mm.

RESULTS

The ranges of shell lengths of the specimens used in this
study and those recorded during a 4-yr study program in
the same sampling localities (unpublished data) are pre-
sented in Table 1.

Considering the residual variance, the best fit to the 10
Ford-Walford plots was given by an AM functional regres-
sion computed following Nair-Bartlett’s procedure
(BARTLETT, 1949). Taking into account the homogeneity
of variances (Bartlett’s test; P > 0.05), an analysis of
covariance (ANCOVA) showed no significant difference
in slopes and intercepts between sexes and sampling pe-
riods (P > 0.05). Consequently, the data were pooled and
a global AM functional regression for each site was cal-
culated.

In all cases the regressions of L,,, on L, were highly

L. F. Guzman & C. F. Rios, 1987

Table 1

Range of shell lengths (mm) of Nacella (P.) magellanica
collected during sampling periods in each study site (I:
October-November 1977; II: January 1978; III: July-
August 1978; IV: December 1978-February 1979). In
parentheses are given the size ranges (mm) of limpets
inhabiting the mid-intertidal zone. Locality codes are given

in Figure 1.

Local- I II Ill IV
ities (Spring) (Summer) (Winter) (Summer)
G 10.9-46.7 10.2-46.5 12.4-43.5 14.2-46.5

(9-48) (7-46) (7-50) (9-48)
S 16.5-47.4 11.0-62.7 15.0-52.5 23.1-44.5
(11-48) (7-62) (13-52) (9-46)
D 17.5-45.0 8.3-54.8 13.8-50.0 15.0-51.0
(14-46) (5-54) (6-53) (12-50)
P 20.5-47.4 11.7-36.2 10.3-43.2 11.3-50.8
(11-48) (7-40) (7-44) (9-50)
W 9.5-60.8 12.7-59.3 14.9-57.5 17.3-56.8
(7-68) (5-64) (3-57) (9-64)
Cc 19.0-41.2 20.4-48.9 14.8-56.9 22.6-42.5
(16-45) (7-50) (13-56) (17-46)
E 37.0-49.2 18.0-51.8 18.9-49.0 10.6-51.9
(33-52) (9-52) (6-50) (7-52)
R 37.0-48.8 16.6-48.8 20.1-49.1 43.5-48.8
(37-52) (13-56) (17-50) (10-50)
B 31.1-42.0 30.8-40.5 17.6-41.3 16.1-41.5
(29-43) (21-42) (13-43) (9-50)
a 13.2-30.8 17.0-31.9
(12-41) (12-32)

* Sampled on April (autumn) and December (spring) 1980,
respectively.

significant and explained over 92% of the observed vari-
ances, reflecting a good predictive relationship. The vari-
ances about the regression lines were heteroscedastic (P >
0.05), although three groups with homogeneous variances
can be segregated; the population at Remo was hetero-
geneous with respect to all others. According to the AN-
COVA applied within each homogeneous group, it is pos-
sible in some cases to calculate a common AM regression
line, although the majority of the regression coefficients
were significantly different (P > 0.05; Table 2).

A lower annual growth rate (slope) was estimated for
the Gregorio and Remo populations, while higher values
were obtained at Wreck-Catalina, reflecting an increasing
tendency from west to east, 7.e., from the interior sites
toward those near the eastern entrance of the Strait. The
shell length at the first year of growth (intercept) follows
an opposite tendency to the slope values, being larger in
the inner sites. The value of the Gregorio population is
almost three times larger than that of Wreck-Catalina.

The results obtained with the von Bertalanffy growth
model reflect different growth rates of the studied popu-
lations. A greater growth rate was found at Gregorio,

Page 161

Table 2

Single and common Ford-Walford regressions for Nacella

(P.) magellanica. b = slope; a = intercept; 7? = determi-

nation coefficient; n = sample size. Locality codes are given
in Figure 1.

Localities b a r n
G 0.826 9.368 0.941 362
R 0.863 7.481 0.974 601
S 0.881 7.964 0.949 432
E-D-B 0.896 6.332 0.964 300
T-P 0.924 4.636 0.963 412
W-C 0.974 3.127 0.991 200

Santiago, and Remo, and the opposite at Wreck-Catalina
(Table 3; Figure 2). The largest specimen collected in each
locality, the theoretical age limit, the instantaneous rate of
natural mortality, and the conditional mortality rate are
also included in Table 3.

Although Wreck-Catalina populations presented the
highest asymptotic length (120 mm) and those at Gregorio
the lowest (54 mm), this parameter did not show a geo-
graphic tendency. According to a two-tailed Spearman
rank correlation test (SNEDECOR & COCHRAN, 1964) the
asymptotic length and the actual maximum size registered
at each sampling site are positively correlated (r = 0.652;
P < 0.05). Von Bertalanffy growth coefficients (K) varied
between 0.0263 and 0.1913, decreasing toward the sites
located near the eastern entrance of the Strait. The higher
K value was determined for Gregorio, and it is approxi-
mately nine times larger than the lowest value recorded
at Wreck-Catalina. The estimated annual growth rate in-
dicated that different ages reached the 95% asymptotic
length (A,); and that these ages ranged between 15 and
37 yr, excluding Wreck-Catalina where the value was
extremely high (113 yr). Because as K increases asymptotic
length decreases, the lowest theoretical age limit was es-
timated for Gregorio, while the highest was determined
for Wreck-Catalina.

The mortality rates were low, varying between 0.026
at Wreck-Catalina (2.6%) and 0.191 at Gregorio (17.4%),
and showing an inverse relationship with growth rate.
Mortality at Gregorio (inner site) was almost seven times
higher than that at Wreck-Catalina (outer sites).

Along the study areas, tidal range shows a clear gradient
from the eastern entrance to the second narrow (approx-
imately from 10 to 4 m during spring tides), and correlates
with the limpet’s annual growth rate, size at the first year
of growth, longevity, and mortality. In contrast, an inde-
pendent relationship between K, L., relative height of
sampling areas, and tidal range at each site (following
Kendall’s nonparametric concordance analysis W = 0.10;
P > 0.05) was found. Annual growth rate, size at the first
year of growth, mortality rate, and asymptotic length are
not correlated with limpet population density (mean val-

Page 162

60

50

+
fo)

LENGTH (mm)
WwW
°

The Veliger, Vol. 30, No. 2

SANTIAGO

GREGORIO
REMO

ESPORA—DELGADA-BAXA

TANDY—POSESION
WRECK-CATALINA
20
10

10 1 12 13 14 15

AGE (YEARS )

Figure 2

Von Bertalanffy growth curves for six populations of Nacella (P.) magellanica in the Strait of Magellan.

ues, unpublished data) according to a two-tailed Spear-
man’s rank correlation test (P > 0.05). These variables,
excluding asymptotic length (P < 0.05), are also indepen-
dent of the intensity of aggregation estimated according to
the Morisita index (SOUTHWOOD, 1975) (P > 0.05; un-
published data).

According to an analysis of variance (ANOVA), the
mean marginal growth for limpets collected during dif-
ferent seasons was significantly different (P < 0.05), being
higher during summer in comparison to spring and winter
seasons (ANOVA; P < 0.05) (Table 4). The largest dif-
ferences were observed between summer and winter, while
no difference was detected between summer periods (P <
0.05). A geographical gradient in marginal growth is also
distinguishable and follows the trend described for the
annual growth estimation, 7.e., a tendency to decrease from
west to east.

The seasonality in mean marginal growth follows the
same pattern observed in some physical and _ biological
growth-related parameters of the Strait (Figure 3). Data
on macroalgal abundance have demonstrated a clear sea-
sonal pattern, with maximum coverage in spring-summer
and minimum coverage in winter (unpublished data). Also,
photoperiod length interpolated from FRANCIS (1972) for
the 52°S latitude is characterized by 17 h in early summer
(December) and 8 hr in winter (July). Meanwhile, the
surface seawater temperatures (from National Petroleum
Company records) show the highest values in February
(11.9°C) and the lowest in August (2.4°C).

DISCUSSION

Several factors can affect age and growth estimates when
they are based on the shell ring method. In our study it
must be noted that (1) limits are imposed by the assumption
that growth ring formation occurs only once a year, and
(2) there are difficulties in assessing consecutive growth
rings, especially at the shell apex.

The criteria adopted to assess consecutive rings seem to
be appropriate according to the determination coefficient
values and the non-significant differences in slopes and
elevations of the Ford-Walford relationships when periods
within each locality were compared. On the other hand,
the difficulty in assessing the first three or four growth
rings is reflected in a poor representation of the left part
of the Ford-Walford plots. In this case, asymptotic length
should be overestimated and growth rhythm could not be
as low as that obtained. Nevertheless, excluding the Wreck-
Catalina estimation, all other cases show the asymptotic
length to be close to the actual maximum size recorded at
each sampling site. The difference between predicted and
actual size at Wreck-Catalina can be explained, as has
been pointed by KNIGHT (1968), by the growth line cur-
vature which mathematically leads to an extremely large
asymptotic length and, consequently, has no biological
meaning.

A seasonal growth pattern in Nacella (P.) magellanica
has not been experimentally shown, but some results sug-
gest that such a pattern might occur in this limpet species.

L. F. Guzman & C. F. Rios, 1987

Page 163

Table 3

Von Bertalanffy parameters for Nacella (P.) magellanica. t, = theoretical age at length zero; K = instantaneous growth
rate; L,, = asymptotic length; A, = 95% theoretical limit age; M = instantaneous rate of natural mortality; A = conditional
mortality rate; LT = maximum recorded length. Locality codes are given in Figure 1.

es A, A LT
Localities (mm) K th (yr) M (%) (mm)
G 54 0.1913 0.00910 15.7 0.191 17.4 55a
R 55 0.1470 0.01153 20.4 0.147 13.7 55n2
S 67 0.1271 0.00910 23.6 0.127 11.9 61.0
E-D-B 61 0.1098 —0.00432 Dies 0.110 10.4 54.7-62.0-51.0
T-P 61 0.0792 —0.00289 37.8 0.079 7.6 41.8-52.0
W-C 120 0.0263 —0.00463 113.9 0.026 2.6 74.7-59.1

In fact, marginal summer growth increments were con-
sistently higher than those estimated for winter and also,
but to a lesser extent, than those of spring. We assumed
that the beginning of ring formation occurs between the
end of summer and early autumn, z.e., between March
and April. Initiation of annulus formation cannot occur
during mid winter, because this would require a very short
lapse of time to explain the relatively high marginal growth
increment of spring samples. Breeding of N. (P.) magel-
lanica in the Strait occurs annually between December and
January (unpublished data), and the formation of a re-
productive growth ring must be discarded because the mar-
ginal growth increment in summer samples is relatively
too high. This seasonality in growth is in concordance with
the annual fluctuation of physical and biological environ-
mental conditions registered in the eastern part of the Strait
of Magellan. Strong seasonal constraints by these factors
(e.g., incident light, temperature, and algal coverage) could
result in restrictions in molluscan shell growth during these
critically limiting months. A seasonal growth pattern has
been observed in a number of marine gastropods (e.g.,
SEAPY, 1966; BRETOS, 1978; McQualIpD, 1981; PHILLIPS,
1981; RAcE, 1981; CocKCROFT & FORBES, 1981; Mc-
LACHLAN & LOMBARD, 1981); but growth rate seasonality
reported for several Antarctic invertebrates as a response
to the marked seasonal fluctuations of physical parameters
is especially enlightening. Among these, the Antarctic lit-

torinid Laevilacunaria antarctica (Martens, 1885) (PICKEN,
1979) and the Antarctic limpet N. (P.) concinna (Strebel,
1908) (PICKEN, 1980) have been reported.

The growth parameters obtained here fall well within
the reported range for several species of marine gastropods,
although Nacella (P.) magellanica can be considered among
those species with a low growth rate. This feature is in
accordance with estimates for N. (P.) concinna (PICKEN,
1980) but differs from N. delesserti (BLANKLEY & BRANCH,
1985), which shows a much higher growth rate. The first
year of growth of N. delesserti is almost four times greater
than the highest estimation obtained for N. (P.) magellan-
1ca.

An inverse relationship between growth rate and lon-
gevity is evident for Nacella (P.) magellanica. This relation
is in agreement with FISHER-PIETTE’s (1941) conclusion
on growth of several European marine species (7.e., the
faster growth, the shorter longevity). A similar inference
was reached by BRANCH (1974) working with five South
African Patella species, demonstrating that this relation-
ship occurs at an intraspecific and interspecific level.

The longevities we report are among the highest re-
corded for marine gastropods (see review by POWELL &
CUMMINS, 1985). It is interesting to point out that, in a
littoral population of the Antarctic limpet Nacella (P.)
concinna, longevity is approximately 21 yrs (PICKEN, 1980),
while in a sublittoral population of the same species, it

Table 4

Mean marginal growth (mm) + SE for Nacella (P.) magellanica at selected sites of the study area. Locality codes are
given in Figure 1.

Oct. ’77 Jan. ’78 Jul.-Aug. °78 Dec. ’78-Feb. ’79
Localities (Spring) (Summer) (Winter) (Summer)
G 0.58 + 0.054 1.14 + 0.155 0.62 + 0.094 1.28 + 0.172
S 0.88 + 0.122 0.96 + 0.098 0.51 + 0.051 1.46 + 0.144
D 0.68 + 0.107 1.18 + 0.156 0.34 + 0.104 1.00 + 0.084
W 0.59 + 0.120 0.65 + 0.070 0.14 + 0.048 0.78 + 0.028
P 0.83 + 0.124 1.13 + 0.104 0.53 + 0.095 0.85 + 0.114
R 0.68 + 0.097 0.89 + 0.097 0.34 + 0.075 0.86 + 0.107

Page 164
mm.
1.5
1. MEAN MARGINAL GROWTH
1.3
VAN
~
11 BS
oi SS.
ea wr.
ZA 7 7 —— Oe SS.
ays >= SS
ae aS —

2. ALGAL COVERTURE

ABIOTIC PARAMETERS

The Veliger, Vol. 30, No. 2

Te)
SANTIAGO oO Pa
a
A a
GREGORIO a wi
DELGADA X a eee
Aa Ae
WRECK Oo i mee
7 —
REMO ry Ya Xx
47 a
POSESION e Ae oe

1978 1979

Figure 3

Mean marginal growth of Nacella (P.) magellanica at different sites of the Strait of Magellan. The seasonal pattern
of some physical and biological growth-related parameters in the study area are included. A®, algal coverage in
In%; B®, solar radiation in Langley/h; CA, photoperiod in hours with an intensity >10 foot candles (107.6 lux);

Dx, surface seawater temperature (°C).

exceeds 60 yr (Shabica, 1976, in PICKEN, 1980). This last
estimate is similar to the longevity of an intertidal popu-
lation of N. (P.) magellanica from Wollaston Island (62
yr, unpublished data). The studied populations from inner
sites, which presented the lowest longevities, showed a
clearly higher longevity than that reported by BLANKLEY
& BRANCH (1985) for Nacella delesserti (8-10 yr) from
Marion Island.

Although mortality rate estimates have a predictive val-
ue, mortality agents probably exert a relatively low pres-
sure on the studied populations. At least three mortality
sources can be mentioned in our case: predation, parasit-
ism, and physical disturbance. Along the studied areas it
has been observed that Anasterias antarctica (Lutkan, 1856)
preys on Nacella (P.) magellanica, but the low density and
relatively small size of this seastar in the sampling area
(personal observations) suggest that predation by this species
is unimportant as a regulating factor. Other characteristic

limpet predators, the sea gull Larus dominicanus (Lichten-
stein) and the oystercatchers Haematopus spp., have been
observed in low density, and restricted to a few sites within
the study area (personal observations). A low predation
pressure has also been suggested by WALKER (1972) for
the Antarctic limpet Patinigera polaris (Hombron & Jac-
quinot) (=Nacella [P.] concinna) at the South Orkney Is-
lands, although L. dominicanus has been mentioned as the
main predator for this species (WALKER, 1972; CASTILLA
& ROZBACZYLO, 1985). On the other hand, BRANCH (1985)
indicates an important role of L. dominicanus preying on
a subantarctic limpet, N. delesserti, with the predator ac-
counting for about 50% of the known annual mortality of
the largest limpets. Parasitism may also contribute to mor-
tality. Limpets at Remo, Baxa, and Tandy showed a vari-
able but unquantified infestation by trematodes of the fam-
ily Gymnophallidae (M. O. de Nunez, personal
communication). As many as 1500 metacercaria have been

L. F. Guzman & C. F. Rios, 1987

found in a single individual (unpublished data). The third
major source of mortality is represented by the rolling of
cobbles and boulders. Although this aspect has not been
evaluated, it likely has a greater influence on the limpet
population dynamics, especially during severe storms.

A number of unknown factors induce an ecological gra-
dient along the study area. For example, the population
density of the mussel Mytilus chilensis (Hupe, 1840) in-
creases substantially from the second narrow toward the
eastern entrance of the Strait (LANGLEY et al., 1980), as
does the species richness of the infauna and epibenthos
(WENDT, 1982; unpublished data). Now we have added
the growth trend of Nacella (P.) magellanica, which is
correlated with tidal range. However, several physical and
biological factors may induce changes in the growth of
gastropods (e.g., BRANCH, 1974; LEwIs & BOWMAN, 1975;
Back, 1977; BRETOS, 1978; McQualID, 1981), suggesting
that the single tidal range-growth relationship we en-
countered may not explain all the geographical growth
trend reported.

ACKNOWLEDGMENTS

We thank Dr. Marta Bretos of Universidad de la Frontera,
Temuco, Chile, for reading and commenting on an early
manuscript. Two anonymous reviewers did much to im-
prove a previous version of this paper. We are also grateful
to Demetrio Diaz and Mario Donoso for field assistance,
and to our colleague Sergio G. Andrade for his cooperation.

LITERATURE CITED

BARTLETT, M.S. 1949. Fitting a straight line when both vari-
ables are subject to error. Biometric 5:207-211.

Biack, R. 1977. Population regulation in the intertidal limpet
Patelloidea alticostata (Angas, 1865). Oecologia 30:1-22.
BLANKLEY, W. O. & G. M. BRANCH. 1985. Ecology of the
limpet Nacella delessert: (Philippi) at Marion Island in the
sub-Antarctic southern ocean. Jour. Exp. Mar. Biol. Ecol.

92:259-281.

BraNncH, G. M. 1974. The ecology of Patella Linnaeus from
the Cape Peninsula, South Africa. 3. Growth rate. Trans.
Roy. Soc. S. Africa 41:161-193.

BRANCH, G. M. 1985. The impact of predation by kelp gulls
Larus dominicanus on the sub-antarctic limpet Nacella deles-
sertt. Polar Biol. 4:171-177.

Bretos, M. 1978. Growth in the keyhole limpet Fissurella
crassa Lamarck (Mollusca: Archaeogastropoda) in northern
Chile. Veliger 21:268-273.

Bretos, M. 1980. Age determination in the keyhole limpet
Fissurella crassa Lamarck (Archaeogastropoda: Fissurelli-
dae), based on shell growth rings. Biol. Bull. 159:606-612.

Bretos, M. 1982. Biologia de Fissurella maxima (Mollusca:
Archaeogastropoda) en el norte de Chile. I. Caracteres gen-
erales, edad y crecimiento. Cahiers Biol. Mar. 23:159-170.

CaRCELLES, A. R. & S. WILLIAMSON. 1951. Catalogo de los
moluscos marinos de la Provincia Magallanica. Mus. Arg.
Cs. Nat. Bernardino Rivadavia, Ciencias Zoologicas 2:225-
383.

CasTILLa, J. C. & N. RozpaczyLo. 1985. Rocky intertidal
assemblages and predation on the gastropod Nacella (Pati-

Page 165

nigera) concinna at Robert Island, South Shetland, Antarc-
tica. Ser. Cient. INACH 32:65-73.

CockcrorT, V. G. & A. T. ForBes. 1981. Growth, mortality
and longevity of Cerithidea decollata Linnaeus (Gastropoda:
Prosobranchia) from Bayhead Mangroves, Durban Bay,
South Africa. Veliger 23:300-308.

DELL, R. K. 1971. The marine Mollusca of the Royal Society
Expedition to southern Chile, 1958-59. Rec. Dom. Museum
7:155-233.

FISHER-PIETTE, E. 1941. Croissance, taille maxima et longevite
possible de quelques animaux intercotidaux en fonction du
millieu. Annls. Inst. Oceanog., Monaco 21:1-28.

FRANCIS, C. A. 1972. Duracion del dia para la reaccion foto-
periodica en plantas. Folleto Tecnico No. 2. Centro Inter-
nacional de Agricultura Tropical, Cali, Colombia. 32 pp.

FRANK, P. W. 1969. Growth rates and longevity of some gas-
tropod mollusks on the coral reef at Heron Island. Oecologia
2:232-250.

GULLAND, J. A. 1965. Manual of methods for fish stock as-
sessment. Part 1. Fish population analysis. FAO Fish. Tech.
Pap. 40, Rev 1. 68 pp.

GuzMAN, L. 1978. Patron de distribucion espacial y densidad
de Nacella magellanica (Gmelin, 1791) en el intermareal del
sector oriental del Estrecho de Magallanes (Mollusca: Gas-
tropoda). Ans. Inst. Pat., Punta Arenas (Chile) 9:205-219.

KNIGHT, W. 1968. Asymptotic growth: an example of nonsense
disguised as mathematics. Jour. Fish. Res. Bd. Canada 25:
1303-1307.

LANGLEY, S., L. GUZMAN & C. Rios. 1980. Aspectos dinamicos
de Mytilus chilensis (Hupe, 1840) en el Estrecho de Magal-
lanes. I. Distribucion, densidad y disposicion espacial en el
intermareal. Ans. Inst. Pat., Punta Arenas (Chile) 11:319-
332)

Lewis, J. R. & R. S. BowMan. 1975. Local habitat induced
variations in the population dynamics of Patella vulgata L.
Jour. Exp. Mar. Biol. Ecol. 17:165-203.

McLacuian, A. & H. W. LOMBARD. 1981. Growth and pro-
duction in exploited and unexploited populations of a rocky
shore gastropod, Turbo sarmaticus. Veliger 23:221-229.

McQualp, C. 1981. Population dynamics of Littorina africana
knysnaensis (Philippi) on an exposed rocky shore. Jour. Exp.
Mar. Biol. Ecol. 54:65-75.

MirANDA, O. 1975. Crecimiento y estructura poblacional de
Thais (Stromanita) chocolata (Duclos, 1823) en la Bahia de
Mejillones del Sur, Chile (Mollusca, Gastropoda, Thaidi-
dae). Rev. Biol. Mar. Dep. Oceanol. Univ. Chile 15:263-
2806.

OTAEGUI, A. V. 1974. Las especies del genero Patinigera Dall
1905 en la Provincia Magallanica (Mollusca, Gastropoda,
Prosobranchiata). Physis B. Aires 33:173-184.

PHILLIPS, D. W. 1981. Life-history features of the marine
intertidal limpet Notoacmea scutum (Gastropoda) in central
California. Mar. Biol. 64:95-103.

PICKEN, G. B. 1979. Growth, reproduction and biomass of the
Antarctic gastropod Laevilacunaria antarctica Martens 1885.
Jour. Exp. Mar. Biol. Ecol. 40:71-79.

PIcKEN, G. B. 1980. The distribution, growth, and reproduc-
tion of the Antarctic limpet Nacella (Patinigera) concinna
(Strebel, 1908). Jour. Exp. Mar. Biol. Ecol. 4:71-85.

PowELL, A. W. B. 1973. The patellid limpets of the world
(Patellidae). Indo-Pacific Mollusca 3:75-206.

PowELL, E. N. & H. Cummins. 1985. Are molluscan maximum
life spans determined by long-term cycles in benthic com-
munities? Oecologia 67:177-182.

Race, M.S. 1981. Field ecology and natural history of Cer-

Page 166

ithidea californica (Gastropoda: Prosobranchia) in San Fran-
cisco Bay. Veliger 24:18-27.

SEAPY, R.R. 1966. Reproduction and growth in the file limpet,
Acmaea limatula Carpenter, 1864 (Mollusca: Gastropoda).
Veliger 8:300-310.

SNEDECOR, G. & W. COCHRAN. 1964. Metodos estadisticos
aplicados a la investigacion agricola y biologica. Compania
Editorial Continental S. A., Mexico. 626 pp.

SOUTHWOOD, T. R. E. 1975. Ecological methods. Chapman
and Hall: London. 391 pp.

TAYLor, C.C. 1959. Cod growth and temperature. Cons. Int.
Explor. Mar. 23:366-370.

VON BERTALANFFY, L. 1938. A quantitative theory of organic
growth (Inquiries on growth laws). II. Human Biology 10:
181-213.

WALFORD, L. 1946. A new graphic method of describing the
growth of animals. Biol. Bull. 90:141-147.

The Veliger, Vol. 30, No. 2

WALKER, A. J. M. 1972. Introduction to the ecology of the
Antarctic limpet Patinigera polaris (Hombron & Jacquinot)
at Signy Island, South Orkney Islands. Brit. Antarct. Surv.
Bull. 28:49-69.

WENDT, A. 1982. Descripcion de comunidades faunisticas in-
termareales de la costa oriental del Estrecho de Magallanes.
Mar. Biol. Tesis, Universidad de Concepcion. 126 pp.

WILbBurR, K. M. & G. OWEN. 1964. Growth. Pp. 211-242. In:
K. M. Wilbur & C. M. Yonge (eds.), Physiology of Mol-
lusca, Vol. I. Academic Press, Inc.

WILLIAMSON, P. & M. A. KENDALL. 1981. Population age
structure and growth of the trochid Monodonta lineata de-
termined from shell rings. Jour. Mar. Biol. Assoc. U.K. 61:
1011-1026.

The Veliger 30(2):167-172 (October 1, 1987)

THE VELIGER
© CMS, Inc., 1987

Herbivory in Juvenile //yanassa obsoleta

(Neogastropoda)

by

GAYLE A. BRENCHLEY

Department of Ecology and Evolutionary Biology, University of California,
Irvine, California 92717, U.S.A.

Abstract.

The mud snail Jlyanassa obsoleta (Say, 1822) is unique among the typically carnivorous

neogastropods in possessing a crystalline style used to digest plant material. While adults are thought
to be obligate omnivores, results of three experiments indicate that juvenile J. obsoleta (4-6 mm shell
height) are herbivores. Juveniles gained body weight and added shell material when fed monocultures
of benthic diatoms (Acanthes brevipes and Nitzschia sp.). Juveniles of both J. obsoleta and the herbivorous
mesogastropod Littorina littorea (Linneaus) grew on diets of sand microflora and a filamentous green
alga (Pilinia lunatiae). Furthermore, interspecific effects of density on growth on a sand-microfloral diet
were similar to intraspecific effects, indicating that juveniles of the two species similarly exploited the
same food items. Because high assimilation efficiency on a plant diet requires style presence, the similarity
between the two species’ growth patterns suggests that young J. obsoleta do not dissolve their styles as
adults do. Herbivory may have permitted young J/. obsoleta, able to compete successfully with herbivorous
mesogastropods, to invade upper intertidal marsh habitats and obtain refuge from crustacean predators.

INTRODUCTION

Ilyanassa obsoleta (Say, 1822) is an abundant and widely
distributed mud snail on intertidal flats along the east coast
of North America. The success of this species is often
attributed to its unusually diverse diet (DIMON, 1905;
SCHELTEMA, 1964; Crisp, 1969; CurTIs, 1980; CurTIs &
HurpD, 1979, 1981a). The species is unique among the
typically carnivorous neogastropods in possessing a crys-
talline style (NOGUCHI, 1921; JENNER, 1956; CuRTIS &
HurbD, 1979). The occurrence of this style is apparently
unique among the gastropods in general in that it under-
goes a cyclic formation and dissolution (ROBERTSON, 1979;
CurTIS, 1980; CurTIs & HuRD, 1981a). The style contains
amylase used to digest plant material (YONGE, 1930;
BROwN, 1969), and during its absence the gut contains
proteases. A digestive rhythm allows the organism to utilize
both plant and animal tissue.

Although it is well known that J/yanassa obsoleta feeds
on benthic algae, CURTIS & HurRD (1979) found that one-
year old individuals (10.8-14.8 mm shell height) grew only
when fed a mixed diet of both meat (shrimp) and vegetable
(spinach). They postulated that the cycling of the crystal-
line style was necessary for the dietary requirements of
the species. The inclusion of carrion in the snail’s diet is
also well known but it is typically a scarce and unreliable

resource. This observation led JENNER (1956) to speculate
that the snail may obtain most of its nutrition from mi-
croorganisms in the sediment. Aptly described as a “‘bio-
logical vacuum cleaner” (CURTIS & HUuRD, 1981a), the
snail consequently needs to swallow large amounts of sed-
iment in order to obtain sufficient quantities of tiny mi-
crobes to sustain obligate omnivory.

There are size constraints to bulk deposit feeding, how-
ever. Recently settled //yanassa obsoleta (<7 mm) can ap-
parently swallow particles of mud (<63 wm) but not coarser
sand grains (LOPEZ, 1980). Like other tiny mud snails,
young J. obsoleta are epistratic grazers, 1.e., they scrape
microbial bacteria and algae attached to surfaces of sand
grains (LOPEZ, 1980). Epistratic grazing is incompatible
with an omnivorous diet requiring the organism to process
bulk quantities of sediment.

A hypothesis not previously tested is that juvenile //y-
anassa obsoleta may not require animal food for growth,
i.e., they are herbivores. Using labeled sediment, LOPEZ
(1980) found that juveniles digested microbial films of
algae and bacteria, but stated that most of the label was
associated with the bacteria. The present study examines
growth of juveniles provided monocultures of benthic dia-
toms as food. The ability to grow on plant diets does not
imply that the snail is normally a strict herbivore in nature,

Page 168

The Veliger, Vol. 30, No. 2

B

— 3

£ field lab
we i Aconthes 9 ® /
(2) ; ’ s Vy),
(S TE Nitzschia G /
Lu = 2 Y,
oO O U7,
= jag /
x oO 4
ac
O LiJ Vi

jag WA
= = f Va
ac a Wi, Hei 4
) or 7 50°
nan uJ Wa Soeer™
Lu fala a ee
= i e: ase é

fe) % og0Qg0000 a ¢
4 8 l2
DAYS DAYS
Figure 1

Growth of two groups of juvenile J/yanassa obsoleta fed monocultures of the diatoms Acanthes brevipes and Nitzschia
sp., or starved (triangles) (key to other symbols in insert). The snails were collected fresh from the field or maintained
in the laboratory. A. Weight change. B. Growth along the aperture. Symbols show means; bars are +1 SD.

however. Consequently, additional experiments compared
the diet of this neogastropod, which uses a crystalline style
to digest plant material, to a mesogastropod, the superorder
of typically herbivorous gastropods. Growth of juveniles
of I. obsoleta was compared to that of juvenile Littorina
littorea (Linnaeus), a herbivorous mesogastropod (LUB-
CHENCO, 1978; HUNTER & RUSSELL-HUNTER, 1983;
WaTSON & NorTon, 1985).

MATERIALS anD METHODS

Juvenile Jlyanassa obsoleta and juvenile Littorina littorea
occur together in sandy marsh habitats in Barnstable Har-
bor, Massachusetts. All snails used in this study were
collected from a marsh tide pool in a sandy habitat (median
grain 0.62 mm, 0.8% silt-clay) near the mouth of the bay.
Each snail was individually numbered on the spire (total,
144 I. obsoleta and 130 L. littorea). To measure new shell
growth, a line was inked on the outer shell surface along
the original aperture edge with a nontoxic ink (Tech-Pen
ink, Mark-Tex Corp., Englewood, New Jersey). The se-
cretion of new shell material was measured from the ink
line using an ocular micrometer (+0.02 mm). Snails were
maintained without food (1) for 36-48 h prior to feeding
or (2) for the duration of each study (controls). All studies
were conducted at temperatures between 20 and 23°C and
at salinities of 31-34%o.

Juvenile Z/yanassa obsoleta were fed monocultures of the
diatoms Acanthes brevipes and Nitzschia sp. in the labo-
ratory. Diatoms were grown under fluorescent light on
autoclaved dishes (14 cm diameter) containing an enriched
seawater medium (HINEGARDEN & TUZZI, 1981:229) and

washed with filtered seawater. Six snails (4-6 mm shell
length) collected fresh from the field in August 1985, or
eight snails (also 4-6 mm) maintained without meat or
carrion at 8-12°C for a year in the laboratory, were placed
into separate dishes. Snails were changed to fresh dishes
every 2 days to minimize growth of bacteria on feces.
Aperture growth and snail weight (+0.002 g) after blotting
the aperture were measured every 4 days for 12 days for
individuals on a diet of Acanthes and subsequently for 12
days on a Nitzschia diet. At the end of the experiment the
new shell material was removed and the snails were re-
weighed. Effects of diet on weight change and aperture
growth of snails were determined by analyses of covariance
using log-transformed data and initial weight and days
lapsed as covariates. Bartlett’s test was used to test for
homogeneity of variances in these and all other ANOVAs.

Growth of juvenile J/yanassa obsoleta (4-6 mm) and ju-
venile Littorina littorea (5-7 mm) was studied in outdoor
seawater tanks in August 1981. Snails were placed into
compartments (4 x 4 x 4 cm) of plastic storage boxes
perforated with numerous holes, too small for the snails
to pass through but adequate for circulation, and main-
tained on the floor of the empty tanks with seawater con-
stantly flowing over them. The snails were collected 36-
48 h prior to the experiments and marked. Twenty control
snails (each species) were maintained indoors without food.
For single-species treatments, 10 snails of one species were
placed into a compartment and provided (1) one living
adult J. obsoleta with a green alga (Pilinia lunatiae) growing
on its shell, (2) 1.5 cm? of diatomaceous sand freshly col-
lected from the marsh pool, or (3) both a shell and 1.5 cm*

G. A. Brenchley, 1987

Page 169

Table 1

Analysis of covariance tables for aperture growth and weight

gain in two groups of juvenile /lyanassa obsoleta on two

diatom monocultures. The covariates are initial shell length
and days lapsed.

Mean
Source df square F ratio
Aperture growth!
Group 1 5.808 47.288***
Diet 1 3.411 ZeiOne*
Interaction 1 0.162 13 15
Covariate 2 2.417 IS) G/F
Error 66 0.123
Weight gain?
Group 1 1.478 2533 OSne
Diet 1 0.496 8.507**
Interaction 1 0.256 4.385*
Covariate 2 1.570 26.947***
Error 74 0.583

#42 < O.OSe “HP < O.Wile +4 1? < OOO,

' Bartlett’s test for homogeneity of variances, x? = 1.614, df =
3, JP > 0.05.

? Bartlett’s test, x? = 2.423, df = 3, P > 0.05.

of sand. Snails were not weighed in this experiment. Com-
parisons of aperture growth [log,.(x + 1)] after 8 days
were made between species and diets by analysis of co-
variance, using shell length as a covariate. The quality
and quantity of plant material on the sand and shells (five
replicates each) were determined by extracting plant pig-
ments overnight in darkness at 4°C with 10 mL of cold,
90% glass-distilled methanol after the methods of FENCHEL
& STRAARUP (1971). Spectral absorbances before and after
acidification were converted to mg pigment per shell or
1.5 cm’ sand using the Parsons-Strickland equations
(STRICKLAND & PARSONS, 1972).

Growth was also measured in two-species communities
to determine if juveniles grazed the same food items. Fresh
sand (1.5 cm’) was provided in compartments containing
(a) 5 (n = 4 compartments), 10 (n = 2), or 20 (n = 1)
juveniles of one species, or (b) equal numbers (5 [n = 2],
10 [n = 2], or 20 [n = 1 compartment]) of both species.
Growth was measured along the aperture after 8 days. By
two-way analyses of covariance, the per capita growth and
the sum growth of each microcosm population (both log
transformed) were compared between species using total
snail density as a covariate.

RESULTS

Juvenile I/yanassa obsoleta gained weight and added shell
material when fed diatom monocultures, but lost weight
and added no shell material when starved (Figure 1). New
shell material accounted for 33% (+11%) of the weight
increase. Field-fresh snails grew significantly more than
laboratory reared snails but both groups grew faster on

CO shell
O mixed

+ control

4 A sand

WN

APERTURE GROWTH (mm)
i)

O +—____ fa,
L/ttorina /lyanassa
Figure 2

Aperture growth over 8 days of juvenile Littorina littorea and
juvenile Jlyanassa obsoleta on diets of sand, Pilinia on mud snail
shells, and both sand and shell; control snails were not fed. Sym-
bols show means; bars are +1 SD. Key to symbols in insert.

Nitzschia than Acanthes (Table 1). A significant interaction
term was due to the large weight gain of field-fresh snails
on the Nitzschia diet.

Juveniles of Zlyanassa obsoleta and Littorina littorea grew
on diets of sand microflora and Pilinia on mud snail shells
(Figure 2). The Pilinia diet was richer in all plant pigments
studied (Table 2). Differences in growth between species
and diets were not significant (Table 3), but the significant
interaction term demonstrated that the species responded
differently to the diets: L. littorea grew slowly on sand but
equally fast on Pilinza and the mixed diet, whereas juvenile
I. obsoleta grew best on a mixed diet and better on sand
than on Pilinia.

In both single and two-species systems, per capita growth
of individuals on a diet of sand declined with density (Fig-
ure 3A) but total growth of microcosm populations re-
mained constant over density (Figure 3B, Table 4). Species
differences were significant: J/yanassa obsoleta grew faster
than Littorina littorea. For per capita growth, interspecific
density effects were not significantly different from intra-
specific effects, and the interaction term was not significant
(Table 4). Thus, individuals grew at similar rates whether
or not neighbors were related. Relative to monocultures,
the total growth was about 50% less in mixed cultures

The Veliger, Vol. 30, No. 2

Page 170

Table 2

Plant pigments (mg) for sand microflora (1.5. cm*) and
shell epiflora (one shell); means and standard deviations
of five replicates.

Shell/

Pigment Sand microflora Shell epiflora sand
Chlorophyll a 1 ss 07 2.8 + 0.2 17/5
Chlorophyll b 0.19 + 0.05 0.24 + 0.05 1.26
Chlorophyll c 0.76 + 0.12 1.18 + 0.06 1.55
Carotenoids 0.70 + 0.05 0.87 + 0.05 1.24

(with 50% more individuals) (Figure 3B). The total pop-
ulation growth of J. obsoleta was more depressed (owing
to a faster growth rate) than that of L. littorea in the mixed
cultures.

DISCUSSION

This study found that juvenile J/yanassa obsoleta added
body and shell material when fed only benthic diatoms.
Because benthic diatoms trigger the planktonic larvae to
settle (SCHELTEMA, 1961), they are likely to be a major
component of the juvenile’s diet. Juveniles can detach algal
and bacterial films from coarse sands (Figure 2; LOPEZ,
1980) and solid surfaces such as rocks (or glass dishes,
Figure 1). However, they have difficulty manipulating fine
silt particles within the buccal cavity (LOPEZ, 1980) and
also do poorly on filamentous algae like Prlinza (Figure 2)
and Enteromorpha (Brenchley, unpublished data) because
their radula is unable to purchase flexible surfaces.
Juvenile J/yanassa obsoleta are strikingly similar to ju-
venile Littorina littorea in sandy habitats of Barnstable
Harbor (Brenchley, unpublished data). Both species settle
into marshes during summer months and attain a similar
size by autumn. The young snails graze on decaying marsh
grasses and ascend marsh vegetation during high tide. De-
spite the propensity of L. /zttorea to graze on hard substrata,

Table 3

Analysis of covariance table for aperture growth (log trans-

formed) of juvenile //yanassa obsoleta and juvenile Littorina

littorea on single and mixed diets of sand and shell epiflora;
the covariate is initial shell length.

Mean PF
Source! df square ratio P
Species 1 0.0047 0.18 0.671
Diet 2 0.0650 2.53 0.089
Interaction 2 0.0842 3.28 0.046
Covariate 1 0.0016 0.06 0.803
Error 50 0.0256

' Bartlett’s test, x? = 5.681, df.=5, P > 0.05.

Isp 2spp
4 llyanassa @ 0°
eres Littorina & A
(=
E 2
: i
Sel ah
fr
©) a 8
= OS
ee °
O
oc A
LJ
an
no)
t

Ol | eae Cian

30 ‘

|
E ‘
£ 25 ’
a
=
= AO
(ag
Oo
qZ 15 9
5 | 1
od
fe)
s h A
5
[tn ala nie
5 fo) 20 40
TOTAL NUMBER OF SNAILS
Figure 3

Aperture growth of juvenile Littorina littorea and juvenile Ily-
anassa obsoleta as a function of total snail density in single and
two-species systems over 8 days on a diet of diatomaceous sand.
A. Per. capita growth over 4-day intervals. B. Total growth of
microcosm populations in 8 days. Symbols show means; bars are
+1 SD. Key to symbols in insert.

e.g., Pilinia on adult mud snail shells (Figure 2), only 7%
of the juveniles compared to 3% of juvenile J. obsoleta occur
on shell substrata in the tide pool; most juveniles of both
species occur on the sandy substrata.

The two taxonomic groups represented here do not nor-

G. A. Brenchley, 1987

Page 171

Table 4

Analysis of covariance tables for aperture growth and total microcosm growth of juvenile J/yanassa obsoleta and juvenile
Littorina littorea on a diet of diatomaceous sand in single and mixed species communities. The covariate is total snail

density.
Source df Mean square F ratio Comments
Per capita growth!
Species 1 1.878 Die DS Aer growth Ilyanassa > Littorina
1 vs. 2 species 1 0.217 3.147 intra = interspecific effects
Interaction 1 1.415 0.021
Covariate 1 2.608 S/o growth decreases with density
Error 145 0.069
Total growth?
Species 1 0.105 150.06*** growth Jlyanassa > Littorina
1 vs. 2 species 1 0.066 94.68*** less growth in mixed cultures
Interaction 1 0.227 32.44*** Ilyanassa grows less in mixed system
Covariate 1 <0.001 0.42 total growth independent of density
Error 15 0.0007

*** P < 0.0001.
' Bartlett’s test, x? = 6.015, df = 3, P > 0.05.
? Bartlett’s test, x? = 5.776, df = 3; P > 0.05.

mally compete for food, owing to a divergence in diet that
began during the Mesozoic. BROWN (1969) and CuRTIS
(1980) have speculated that the ancestral stock of I/yanassa
obsoleta could not compete with its more specialized, car-
nivorous neogastropod relatives, nor with the more efh-
cient, microherbivorous mesogastropods. Presumably,
digestion of plant foods in the neogastropod stock was
dependent upon an innovation, z.e., style acquisition. Re-
sults of this study suggest that because of this innovation,
young J. obsoleta exploit the same foods as the mesogas-
tropod Littorina littorea. If the density effects of Figure 3
were due to interference, e.g., stress due to crowding, then
the total growth of microcosm populations should have
declined with increased density, but such trends were not
significant (Table 4). Studies of sympatric gastropods have
shown that unrelated species exploit algae differently while
congeners often have similar exploitation abilities (re-
viewed by BRANCH, 1984). The similarities in per capita
growth curves in single versus mixed systems of young /.
obsoleta and L. littorea (Figure 3A) imply equal exploitative
ability, providing the first example for unrelated species.

The results strongly suggest that the young Jlyanassa
retain rather than cycle their crystalline style. Because
algae cannot be digested when the style is absent, disso-
lution of the style would greatly reduce assimilation eff-
ciency on a plant diet. However, the similarity in growth
patterns (Figure 3A) indicates that the mud snail was as
efficient in assimilating plant foods as the littorinid. There
is limited evidence that young //yanassa in marsh habitats
may not cycle their styles (CURTIS & HuRD, 1981b), in
contrast to the cyclic pattern frequently reported for large
(16-25 mm), sexually mature snails (e.g., CURTIS & HuRD,
1981a, b).

Several workers have speculated that the success of J/-
yanassa is due to a diverse diet, yet few have suggested how
the style innovation could enhance the species’ abundance.
In addition to possible costs associated with the formation
or dissolution of the style, the style cycling is quite costly
to adult snails because much ingested material passes un-
digested. CURTIS & HuRD (1981a) relate the species’ suc-
cess to its unique role in the benthic community. Despite
a unique niche, the species’ broad diet does not eliminate
the adults’ reproductive need for carrion (HURD, 1985),
and the style innovation places the juveniles in competition
with herbivorous snails (this study). An explanation not
previously suggested is that the innovation allows the snail
to invade (new) habitats and thereby avoid predators.

Studies of the snail’s ecology in Barnstable Harbor sug-
gest that only asa herbivore can the young //yanassa occupy
a predator refugium in sandy intertidal habitats. The me-
sogastropods and littorinids in particular are tolerant of
desiccation and thus can obtain refuge from most predators
by inhabiting the upper tidal zones. The neogastropods
are less tolerant of desiccation; most nassarlids of temperate
sand flats remain near or below mean low water and only
the adults move into the intertidal zone (e.g., KUSKINS &
MancuM, 1971; TALLMARK, 1980). Adult J. obsoleta are
more tolerant of desiccation than the young (SCHAEFER et
al., 1968) and immune from attack by the shell-crushing
crustaceans of the lower tide zones (BRENCHLEY, 1982,
unpublished data). Susceptible to desiccation and partic-
ularly to crab predators, young /. obsoleta obtain refuge by
settling into upper intertidal pools, seeps, and creek beds.
Herbivory may be a prerequisite for marsh habitation, as
drift carrion is scarce; the snails emigrate to the sand flats
upon reaching maturity (Brenchley, unpublished data).

Page 172

Consequently, the style innovation may permit young snails
to enter a predator refugium, which may partly explain
the numerical success of this ubiquitous species.

ACKNOWLEDGMENTS

The outdoor seawater tanks were provided by the Woods
Hole Oceanographic Institution. I thank Merryl Alber for
assisting in the growth studies, Naomi Culp in the pigment
analyses, Patrick Leahy for providing diatom cultures, and
Peter Dixon for identifying Pilinia. Roger Griffis, Larry
Curtis, and Lynn Carpenter provided helpful comments
on the manuscript. The research was supported in part by
a faculty grant from the University of California, Irvine.

LITERATURE CITED

BrancuH, G.M. 1984. Competition between marine organisms:
ecological and evolutionary implications. Oceanogr. Mar.
Biol. Ann. Rev. 22:429-593.

BRENCHLEY, G. A. 1982. Predation on encapsulated larvae by
adults: effects of introduced species on the gastropod J/yanassa
obsoleta. Mar. Ecol. Prog. Ser. 9:255-262.

Brown, S.C. 1969. The structure and function of the digestive
system of the mud snail, Nassarius obsoletus (Say). Malacol-
ogy 9:477-500.

Crisp, M. 1969. Studies on the behavior of Nassarius obsoletus
(Say) (Mollusca, Gastropoda). Biol. Bull. 136:355-373.
Curtis, L. A. 1980. Daily cycling of the crystalline style in
the omnivorous, deposit-feeding estuarine snail J/yanassa ob-

soleta. Mar. Biol. 59:137-140.

Curtis, L. A. & L. E. Hurp. 1979. On the broad nutritional
requirements of the mud snail, J/yanassa (Nassarius) obsoleta
(Say), and its polytrophic role in the food web. Jour. Exp.
Mar. Biol. Ecol. 4:1-9.

Curtis, L. A. & L. E. Hurp. 1981a. Nutrient procurement
strategy of a deposit-feeding estuarine neogastropod, Ily-
anassa obsoleta. Estuarine Coast. Shelf Sci. 13:277-285.

Curtis, L. A. & L. E. Hurp. 1981b. Crystalline style cycling
in Ilyanassa obsoleta (Say) (Mollusca: Neogastropoda): fur-
ther studies. Veliger 24:91-96.

Dimon, A.C. 1905. The mud snail: Nassa obsoleta. Cold Spring
Harbor Monogr. 5:1-50.

FENCHEL, T. & B. J. STRAARUP. 1971. Vertical distribution
of photosynthetic pigments and the penetration of light in
marine sediments. Oikos 22:172-182.

HINEGARDEN, R. T. & M. M. R. Tuzzi. 1981. Laboratory

The Veliger, Vol. 30, No. 2

culture of the sea urchin Lytechinus pictus. Pp. 291-302. In:
National Research Council, Marine Invertebrates. National
Academy Press: Washington, D.C.

HuntTErR, R. D. & W. D. RUSSELL-HUNTER. 1983. Bioener-
getic and community changes in intertidal Aufwucks grazed
by Littorina littorea. Ecology 64:761-769.

Hurpb, L. E. 1985. On the importance of carrion to reproduc-
tion in an omnivorous estuarine neogastropod, I/yanassa ob-
soleta (Say). Oecologia 65:513-515.

JENNER, C. E. 1956. The occurrence of a crystalline style in
the marine snail, Nassarius obsoletus. Biol. Bull. 111:304.

Kuskins, L. J. & C. P. Mancum. 1971. Responses to low
oxygen conditions in two species of the mud snail Nassarius.
Comp. Biochem. Physiol. 39A:421-435.

LUBCHENCO, J. 1978. Plant species diversity in a marine in-
tertidal community: importance of herbivore food preferences
and algal competitive ability. Amer. Natur. 112:23-39.

Lopez, G. R. 1980. The availability of microorganisms at-
tached to sediment as food for some marine deposit-feeding
molluscs, with notes on microbial detachment due to the
crystalline style. Pp. 387-405. In: K. R. Tenore & B. C.
Coull (eds.), Marine benthic dynamics. Univ. South Caro-
lina Press: Columbia.

Noguchi, H. 1921. Cristispira in North American shellfish. A
note on a spirillum found in oysters. Jour. Exp. Med. 34:
295-315.

ROBERTSON, J. R. 1979. Evidence for tidally correlated feeding
rhythm in the eastern mud snail, //yanassa obsoleta. Nautilus
93:38-40.

SCHAEFER, C. W., N. L. LEVIN & P. MILcH. 1968. Death
from desiccation in the mud-snail, Nassarius obsoletus: effects
of size. Nautilus 82:28-31.

SCHELTEMA, R. S. 1961. Metamorphosis of the veliger larvae
of Nassarius obsoletus (Gastropoda) in response to bottom
sediment. Biol. Bull. 120:92-108.

SCHELTEMA, R.S. 1964. Feeding habits and growth in the mud
snail Nassarius obsoletus. Chesapeake Sci. 5:161-166.

STRICKLAND, J. D. H. & T. R. Parsons. 1972. A practical
handbook of seawater analysis. Fish. Res. Bd. Canada, Bull.
167.

TALLMARK, B. 1980. Population dynamics of Nassarius retic-
ulatus (Gastropoda, Prosobranchia) in Gullmar Fjord, Swe-
den. Mar. Ecol. Prog. Ser. 3:51-62.

Watson, D. C. & T. A. NorTON. 1985. Dietary preferences
of the common periwinkle, Littorina littorea. Jour. Exp. Mar.
Biol. Ecol. 88:193-211.

YONGE, C.M. 1930. The crystalline style of the Mollusca and
a carnivorous habitat cannot normally co-exist. Nature 125:
444-445,

THE VELIGER
© CMS, Inc., 1987

The Veliger 30(2):173-183 (October 1, 1987)

Starvation Metabolism in the Cerithiids
Cerithidea (Cerithideopsilla) cingulata (Gmelin) and
Cerithium coralium Kiener
by

Y. PRABHAKARA RAO, V. UMA DEVI, ann D. G. V. PRASADA RAO

Department of Zoology, Andhra University, Waltair 530 003, India

Abstract. The effect of starvation has been investigated in two tropical cerithiids, Cerithidea (Cer-
ithideopsilla) cingulata (Gmelin, 1790) and Cerithium coralium Kiener, 1841. There was no mortality
up to 28 days in Cerithidea cingulata and 14 days in Cerithium coralium; 50% mortality was recorded
at 98 and 38 days in Ceritthidea cingulata and Cerithium coralium respectively. Water content did not
change significantly (P > 0.05) in either species during starvation. The body component indices of both
species were found to decrease gradually with the period of starvation. Significant changes (P < 0.05)
in the level and content of all the biochemical constituents (viz. carbohydrates, glycogen, protein, total
ninhydrin positive substances [TNPS] and lipids) were observed in different body components of both
the animals during starvation. Among the three tissues examined, the gonad-digestive gland complex
contributed greatly to energy needs when the animals were exposed to starvation. “Carbohydrate-
oriented” metabolism was noticed in both species. Cerithidea cingulata preferred lipids next to carbo-
hydrates while Cerithium coralium utilized proteins after carbohydrates in all the body components.

During starvation, oxygen consumption exhibited a decreasing tendency (P < 0.05) when considered

per snail or per tissue weight in both species. Starvation also decreased the intercept values “a

(recalculated) in both species.

INTRODUCTION

Cerithidea (Cerithideopsilla) cingulata (Gmelin, 1790) and
Cerithium coralium Kiener, 1841, inhabit the backwaters
of Bhimilipatnam on the east coast of India (83°28’E,
17°54'N), 35 km north of Visakhapatnam. There is an
extensive, shallow backwater region adjoining the coast
covering an area of 4.5 km’. A small river, Gousthani, and
three freshwater creeks empty themselves into the back-
water system. The backwater is connected to bay waters
through a narrow entrance channel. The substratum of
the backwater system is composed of medium-sized grains
of sand (0.350-0.250 mm diameter). Cerithidea cingulata
is found in the upper and middle reaches of the backwater
system. During the hot weather season (March-June),
these areas are partly dried up and stagnation occurs more
frequently. Cerithium coralium inhabits the lower reaches
of the backwaters where there is an abundant supply of
algae and diatoms. The hydrographical conditions in the
habitat of these two cerithiids also exhibit wide fluctuations

e699

and, thus, they come from ecologically distinct regions
(PRABHAKARA Rao, 1981). Therefore, several investiga-
tions have been carried out to understand the nature of
the species’ physiological adaptations by exposing them to
temperature (PRABHAKARA RAO & PRASADA Rao, 1983a),
salinity (PRABHAKARA RAO & PRASADA Rao, 1981, 1984a),
oxygen tension (PRABHAKARA RAO & PRASADA Rao,
1983b), and atmospheric oxygen (PRABHAKARA RAo &
PRASADA Rao, 1983c, d). In addition, the availability of
food needed for growth and reproduction also plays a dom-
inant role in the above system (PRABHAKARA Rao, 1981).
Because these snails occur in large numbers in the field,
there is a possibility of depletion of food resources. The
closure of the operculum during adverse environmental
conditions (PRABHAKARA Rao & PRASADA Rao, 1981) may
also force these animals to starve for brief periods. There-
fore, the present investigation was initiated to study the
utilization of body biochemical constituents of Cerithidea
cingulata and Cerithium coralium by subjecting them to
starvation.

Page 174

The Veliger, Vol. 30, No. 2

Table 1

Rates of oxygen consumption and mortality in Cerithidea cingulata and Cerithium coralium at different intervals of starvation
(a: % mortality; b: oxygen consumption wL O,/h + SD and % decrease over initial value; c: weight specific oxygen
consumption wL O,/mg/h + SD and % decrease over initial value; d: log “‘a” intercept values). n = 10; F-test, * P <

Cerithidea cingulata

No. of
days a b c d
0 0 111.00 + 4.77 2.8460 + 0.1223 1.0011
7 0 107.62 + 3.18 2.8320 + 0.0837
3.05 0.50
14 0 VELA ae 5,12 2.1840 + 0.1463 0.8391
31.14 23.26
21 0 66.52 + 2.16* 2.0788 + 0.0675
40.07 26.96
28 0 56.14 + 3.04* 2.0050 + 0.1086
49.42 29.55
38 20 46.72 + 4.01* 1.7969 + 0.1542*
57.91 36.86
48 23 S884 Sill 1.6183 + 0.1571*
65.01 43.14
68 35 29.12 + 2.46* LBAXG sz ONS
73.77 53.49
98 50 20.10 + 1.89* 1.0090 + 0.0945*

81.89 64.55

MATERIALS anp METHODS
Experimental Animals

Animals of both the species, Cerithidea cingulata and
Cerithium coralium, were collected from the backwaters of
Bhimilipatnam. Care was taken to select animals of ap-
proximately the same size (38 to 42 mg of dry weight of
soft parts). They were brought to the laboratory and were
cleaned thoroughly before using them for experimental
work. Then they were equilibrated to laboratory conditions
in an aquarium containing seawater (32%) at 25 + 0.5°C
for 24 h.

During the first phase of the experiment, the effect of
starvation was studied on the mortality rate of both the
species. For this study, 100 animals of each species were
placed in two different aquaria filled with Whatman-42
filtered seawater. The filtered seawater was aerated con-
tinuously and the water was changed daily. At 98 days of
starvation 50% mortality was observed for Cerithidea cin-
gulata and at 38 days of starvation for Cerithium coralium.

Sampling Technique

Changes in the biochemical constituents were studied
by taking a set of 175 animals of each species in two
different aquaria. Ten animals from each set were sacri-
ficed to serve as controls (0 day). The rest of the animals
were exposed to starvation stress as just described. The
intervals at which successive samples of 10 each were taken
for biochemical analysis were arranged depending on the
mortality data of each species.

Cerithium coralium

a b Cc d

0 68.00 + 3.54 1.9714 + 0.1011 0.6551

0 65.56 + 2.12 1.9570 + 0.0633 0.6328
4.99 0.73

0 55.04 + 1.77* 1.8979 + 0.0610 0.5569
20.23 0.11

13 46.08 + 2.03* 1.8808 + 0.0829 0.4797
33.22 0.13

27 32.18 + 3.64* 1.7878 + 0.2022 0.3238
53.36 7.80

50 16.28 + 4.07* 1.0853 + 0.2713* 0.0279
76.41 44.95

The experimental animals, after sacrificing at each in-
terval, were dissected into body components, viz., foot,
gonad-digestive gland complex (GDG complex) and vis-
cera. The above body components were pooled separately
for Cerithidea cingulata and Cerithium coralium. Because
the gonad and digestive gland were found to be closely
associated, they were taken together as the GDG complex.
The different body components were weighed before and
after drying in an oven at 90°C for 48 h to get wet and
dry weights respectively. Then they were powdered and
preserved in clean, dry glass vials placed in a desiccator.
This dry powder was used for the estimation of total car-
bohydrates, glycogen, proteins, total ninhydrin positive
substances (TNPS) and lipids.

Biochemical Analysis

Total carbohydrates and glycogen were estimated by the
method of CARROL et al. (1956). Lowry et al. (1951) was
used for the determination of proteins. Total free amino
acids were represented as total ninhydrin positive sub-
stances (TNPS) and these were estimated by using the
method of Moore & STEIN (1954). The procedure of
chloroform: methanol (2:1) extraction was adopted for
quantification of lipids (FOLCH et al., 1957).

Biochemical Level and Content

The level of each biochemical class is presented on a
milligram per gram dry weight basis. Nutrient content is
calculated by multiplying the level times the body com-

Y. Prabhakara Rao et al., 1987

Page 175

Table 2

Effect of starvation on the water content and body component indices of Cerithidea cingulata and Cerithium coralium
(a: % water content; b: body component index).

Cerithidea cingulata

NoveE Foot GDG complex Viscera

days a b a b a
0 82 +3 0.791 75) 2 2 3.22 13 se 2
7 81 +2 0.776 7443 3.12 Vise il
14 80 + 3 0.761 Ti = 2 3.00 TB a2 2
21 81+1 0.741 TV 3 2.86 V7 we 3
28 82 + 3 0.719 70 +3 2.74 16. a5 2
38 719 + 4 0.699 IQ a= 2 2.58 Vy se 2
48 Wi se 3 0.659 69 +2 2.43 16-2 il
68 US se 4 0.614 68 + 4 2.22 75) s= 3
98 UWS 22 3 0.549 66+5 1.93 7G se PD

ponent index (the relative size of the particular body com-
ponent on a weight basis for a hypothetical 100-g animal;
dry weight of component/weight of the animal x 100)
and expressed in grams (STICKLE, 1975).

Respiration

For each species, 10 animals of uniform size (as de-
scribed earlier) were chosen and numbered serially from
1 to 10. After determining their initial oxygen consump-
tion, they were placed in Whatman-42 filtered seawater
(salinity 32%o, pH 8) for starvation. The animals of each
species were maintained separately in glass troughs at a
temperature of 25 + 0.5°C with continuous aeration. Res-
piration of each species was studied individually at the
same intervals of starvation at which biochemical samples
were taken. Oxygen consumption of the animals was de-
termined every 2 h over a period of 6 h by adopting the
same method used by PRABHAKARA RAO & PRASADA RAO
(1983c). Dissolved oxygen was estimated by using the
Winkler method.

Statistical Evaluation

The values are given as the mean + 1 SD. One-way
analysis of variance (ANOVA) (SNEDECOR & COCHRAN,
1967) was employed to determine the significance of vari-
ation in biochemical level and content during starvation.
The data were studied further by using Duncan’s Multiple
Range Test (SNEDECOR & COCHRAN, 1967). The same
test was also used for the comparison of respiratory rates
at different intervals of starvation.

RESULTS

Table 1 represents the mortality rates of Cerithidea cin-
gulata and Cerithium coralium at different periods of star-
vation. In Cerithidea cingulata, there was no mortality up
to 28 days of starvation, whereas mortality started at 21
days of starvation in Cerithium coralium. It is also inter-
esting (Table 1) that the periods at which 50% mortality

Cerithium coralium

Foot GDG complex Viscera
a b a b a b
80+2 0.769 M45 31011 7744 4.69
80+3 0.749 US 25) Asesi/ 7645 4.60
80+2 0.728 WO a3 Defi Th EA a5 4
Soil 0.709 SOF 2 2556 81+ 4 4.43
SRS OFG85 DS 250 80+3 4.18
80 + 1 0.653 Uae Ah lO) 8242 3.84

occurred were different: 98 days of starvation for Cerithidea
cingulata and 38 days for Cerithium coralium. The rest of
the experiments were designed based on these results.

The percentage water contents of both species at dif-
ferent intervals of starvation are presented in Table 2.
ANOVA reveals no significant difference (P > 0.05) in
these values in all the body components of both the animals
exposed to starvation. However, the percentage water con-
tent of all the tissues was found to be slightly higher in
Cerithidea cingulata than Cerithium coralium (Table 2).
The body component indices of both the animals are shown
in Table 2. In both species there was a gradual decrease
in the indices of different body components as starvation
progressed and this decrease was high in the GDG complex
(40% in Cerithidea cingulata and 30% in Cerithium cora-
lium) when compared to the foot and viscera.

Biochemical Level

Figures 1-3 depict the changes in the level of biochem-
ical constituents in the foot, GDG complex, and viscera
respectively. Significant variations (ANOVA, P < 0.05)
were found in all the biochemical constituents of different
body components, and the data were further subjected to
Duncan’s analysis.

Foot: A significant decrease (P < 0.05) in total carbo-
hydrates started from 28 days of starvation in Cerithidea
cingulata and 21 days of starvation in Cerzthium coralium
(Figure 1). The glycogen values decreased significantly
(P < 0.05) from 38 days of starvation in Certthidea cin-
gulata and 14 days of starvation in Cerithium coralium. The
proteins of both the species followed the same trend as that
of carbohydrates. A significant increase (P < 0.05) in the
TNPS was observed from 14 days of starvation in Ceri-
thidea cingulata and Cerithium coralium. The lipids started
to decrease significantly (P < 0.05) from 48 days of star-
vation in Cerithidea cingulata. In Cerithium coralium, the
significant (P < 0.05) decrease in lipids occurred from 21
days of starvation.

Page 176

aS
O

e)
fe)

mg/g ORY WEIGHT
(oy) 0
O ©

aS
O

Kmol/g
DRY WEIGHT

mg/g
ORY WEIGHT

100

The Veliger, Vol. 30, No. 2

CARBOHYDRATES

GLYCOGEN

PROTEIN

LIPIDS

50 60 70 80 90 iKeXe)

NUMBER OF DAYS

Figure 1

Changes in the levels of different biochemical constituents in the foot of Cerithidea cingulata (

coralium (----- ). Vertical bars represent 1 SD.

GDG complex: In Cerithidea cingulata, the carbohydrates
began to decrease significantly (P < 0.05) from 7 days of
starvation and continued up to 98 days (Figure 2). The
carbohydrates of Cerithium coralium exhibited a significant
decrease (P < 0.05) from 14 days of starvation (Figure
2). The glycogen levels of both the species showed a sig-
nificant fall (P < 0.05) from 21 days of starvation. The
proteins of Cerithidea cingulata decrease little and the sig-
nificant decrease was observed (P < 0.05) from 68 days
and 98 days of starvation. TNPS values exhibited a sig-
nificant increase (P < 0.05) from 14 days of starvation in
Cerithidea cingulata and Cerithium coralium. The lipids of

) and Cerithium

Cerithidea cingulata started to decrease significantly from
48 days of starvation, but there was a significant decrease
(P < 0.05) in the lipid content of Cerithium coralium from
the 7th day onwards.

Viscera: The carbohydrates and glycogen of Cerithidea
cingulata exhibited a significant decrease from 28 days and
48 days of starvation respectively. In contrast, a significant
fall (P < 0.05) in the quantities of carbohydrates and
glycogen was noticed from 21 days of starvation in Ceri-
thium coralium. In Cerithidea cingulata, the protein content
started to decrease significantly from 21 days of starvation

Y. Prabhakara Rao et al., 1987

mg/g DRY WEIGHT

FE
as
ne
=>
(oe)
eS
34>
x
(a)
ke
ae
o
35
Le))
E
>
ax
oO

ie) Ke) 20 30 40

Page 177

CARBOHYDRATES

GLYCOGEN

PROTEIN

LIPIDS

50 60 70 890 30 100

NUMBER OF DAYS

Figure 2

Changes in the levels of different biochemical constituents in the GDG complex of Cerithidea cingulata (
Cerithium coralium (----- ). Vertical bars represent 1 SD.

and TNPS quantities increased significantly from 14 days
of starvation. A significant fall (P < 0.05) in the quantities
of protein from 7 days of starvation coincided with the
significant increase in TNPS values of Cerithium coralium.
The lipid values of Cerithidea cingulata and Cerithium co-
raltum showed a fall in their levels from 38 days and 21
days of starvation respectively.

Biochemical Content

Tables 3-5 present data on the different body biochem-
ical contents of Cerithidea cingulata and Cerithium coralium
at different periods of starvation. ANOVA showed sig-

) and

nificant variations (P < 0.05) in biochemical composition
during different periods of starvation. Duncan’s analysis
further proved (Tables 3-5) that carbohydrates, glycogen,
proteins, and lipids decreased significantly (P < 0.05) with
increasing periods of starvation in different body compo-
nents of both the species. It is evident from Tables 3-5
that there are differences in the periods from where the
significant decrease (P < 0.05) starts. There are also dif-
ferences in these periods not only between levels and con-
tents but also between the two species. However, TNPS
content showed an increase in both the species with in-
creasing starvation period (Tables 3-5).

Page 178

at

mg/g DRY WEIGHT

Kmol/g
DRY WEIGHT

mg/g
DRY WEIGHT

The Veliger, Vol. 30, No. 2

CARBOHYDRATES

GLYCOGEN

PROTEIN

LIPIDS

50 60 70 80 90 100

NUMBER OF DAYS

Figure 3

Changes in the levels of different biochemical constituents in the viscera of Cerithidea cingulata (

coralium (----- ). Vertical bars represent 1 SD.

Respiration

The respiratory rates of Cerithidea cingulata and Cen-
thium coralium were studied at different intervals of star-
vation (Table i). It is evident from the table that the
percentage decreases in oxygen consumption are gradual
with increases in the period of starvation in both the an-
imals when calculated on a per animal basis. Duncan’s
Multiple Range Test revealed significant decreases (P <
0.05) in the oxygen consumption rates from day 14 of
starvation in both the species (Table 1). When the oxygen

) and Cerithium

consumption values are presented on a tissue weight basis
(tissue weight is deduced from the percentage decrease in
dry tissue weight during starvation), the decrease, although
gradual, is not as much as that of the per animal values
in both the species (Table 1). The intercept values of log
“a” in both the animals presented in the table are calcu-
lated using the exponential equation Y = aW?, in which
the regression coefficient “b” is taken from earlier inves-
tigations (PRABHAKARA RAO & PRASADA Rao, 1984b). It
is clear from the table that there is a gradual decrease in
the log “a” values as starvation progresses in both species.

Y. Prabhakara Rao et al., 1987

Page 179

Table 3

Effect of starvation on the content of different biochemical constitutents in the foot of Cerithidea cingulata (a) and Cerithium
coralium (b). All values are expressed as g/100 g dry weight of the tissue + SD except TNPS (m mol/100 g dry weight
of the tissue + SD). F-test, * P < 0.05.

NG Carbohydrates Glycogen Proteins TNPS Lipids
days a b a b a b a b a b
0 0.120 0.092 0.081 0.076 0.409 0.350 0.0027 0.0018 0.161 0.154
+0.005 +0.004 +0.003 +0.005 +0.010 +0.012 +0.0008 +0.0007 +0.010 +0.005
7 0.115 0.085 0.077 0.070 0.389* 0.332 0.0034* 0.0030 0.154 0.147*
+0.004 +0.005 +0.002 +0.007 +0.009 +0.010 +0.0009 +0.0010 +0.009 +0.003
14 0.108 0.076* 0.072 0.063 ON 72% 0.311 0.0046* 0.0032* 0.145 0.138*
+0.003 +0.007 +0.005 +0.005 +0.008 +0.010 +0.0009 +0.0009 +0.011 +0.005
21 0.101 0.068* 0.066 0.057* 0.350* 0.290* 0.0046* 0.0033* 0.139 0.130*
+0.005 +0.005 +0.003 +0.003 +0.009 +0.009 +0.0010 +0.0009 +0.010 +0.002
28 0.093 0.056* 0.061* 0.046* 0.329* 0.267* 0.0046* 0.0040* 0.124* 0.120*
+0.004 +0.007 +0.003 +0.003 +0.009 +0.009 +0.0010 +0.0008 +0.008 +0.003
38 0.083 0.039* 0.054* 0.029* 0.308* 0.221* 0.0052* 0.0042 0.113* 0.101*
+0.003 +0.006 +0.004 +0.005 +0.009 +0.008 +0.0009 +0.0009 +0.009 +0.005
48 0.070* 0.046* 0.268* 0.0062* 0.094*
+0.005 +0.003 +0.010 +0.0007 +0.007
68 0.057* 0.038* 0.230* 0.0066* 0.079*
+0.003 +0.002 +0.009 +0.0009 +0.009
98 0.038* 0.027* 0.191* 0.0066* 0.063*
+0.004 +0.002 +0.006 +0.0008 +0.007
DISCUSSION

The results clearly indicate that the effect of starvation is
not much during the early stages in both species. The
differences in the periods at which the mortality started
(35 days in Cerithidea cingulata and 21 days in Cerithium
coralium) reveal that the former can better tolerate star-
vation stress than the latter. This is further evidenced by
the data that 50% mortality occurred at 98 days in Cer-
ithidea cingulata and 38 days in Cerithium coralium. The
reason may be their distribution: Cerithium coralium occurs
towards wave-swept regions where there is abundant sup-
ply of food in the form of algae and diatoms while Cerith-
idea cingulata lives in the upper reaches of the estuary
where there is less possibility for the growth of algae and
other vegetation (PRABHAKARA RAO, 1981). Cerithidea cin-
gulata may have a better inherent capacity for tolerance
to starvation than Cerithium coralium because the body
biochemical constituents were found to be higher in the
former than the latter. Several other species of mollusks
have been found to survive for various periods when ex-
posed to starvation. In Nucella lamellosa, 90% survival was
reported during 53 days of starvation (STICKLE & DUERR,
1970); Morula granulata exhibited 50% mortality in 70
days of starvation (UMA DEviI et al., 1986); and 90% sur-
vival was observed during 50 days of starvation in La-
mellidens marginalis (MASTANAMMA & RAMAMURTI, 1983).

There is no significant variation (P > 0.05) in the per-
centage water content of different body components in the

two species studied. This is possibly due to the higher
proportion of bound water in the soft parts of the animal
and this may be used for metabolic adjustments during
starvation. A similar condition was reported in Paratel-
phusa hydrodromus when exposed to starvation (KOTAIAH
& RAJABAINAIDU, 1973). Another reason for this insig-
nificant change in the water content may be the presence
of higher quantities of free amino acids in both the ceri-
thiids (PRABHAKARA RAO & PRASADA RAO, 1983b); these
free amino acids can retain water and prevent its escape
from the soft parts of the animal. In Morula granulata also,
no changes in the percentage water content were recorded
during starvation (UMA DEVI et al., 1986).

The present investigation suggests that the GDG com-
plex serves as a storage organ in both species. The GDG
complex indices in both species showed tremendous de-
creases when compared to the foot and viscera. Decreases
in body component indices have also been reported in
several other mollusks—WNucella lamellosa (STICKLE, 1971),
Morula granulata (UMA DEVI et al., 1986), Thais haema-
stoma (BELISLE & STICKLE, 1978), Katharina tunicata (GIESE
& Hart, 1967; HIMMELMAN, 1978), Chiton tatricus (NA-
GABHUSHANAM & DESHPANDE, 1982) and Cryptochiton
stelleri (LAWRENCE et al., 1965)—-when food reserves are
utilized for energy purposes.

From Figures 1-3 and Tables 3-5, it is clear that the
different biochemical constituents (viz., carbohydrates, gly-
cogen, proteins and lipids) which form the reserve food

Page 180 dhe Veliger) Voles 0sNeowZ

Table 4

Effect of starvation on the content of different biochemical constituents in the GDG complex of Cerithidea cingulata (a)
and Cerithium coralium (b). All values are expressed as g/100 g dry weight of the tissue + SD except TNPS (m mol/
100 g dry weight of the tissue + SD). F-test, * P < 0.05.

No. of Carbohydrates Glycogen Proteins TNPS Lipids
days a b a b a b a b a b
0 0.808 0.533 0.622 0.406 0.911 0.698 0.013 0.009 1.159 0.930
+0.045 +0.024 +0.039 +0.030 +0.052 +0.030 +0.003 +0.003 +0.032 +0.036
7 0.711 0.456 0.543 0.353 0.855* 0.626 0.016* 0.015 1.035* 0.358
+0.019 +0.017 +0.031 +0.029 +0.037 +0.023 +0.003 +0.004 +0.034 +0.032
14 0.621 0.371 0.492 0.290 0.786* 0.545 0.018* 0.020 1.029* 0.764
+0.036 +0.022 +0.030 +0.033 +0.045 +0.019 +0.004 +0.003 +0.030 +0.024
21 0.529 0.312 0.446* 0.236 0.724* 0.476 0.025* 0.024 0.941* 0.666
+0.029 +0.028 +0.034 +0.023 +0.037 +0.023 +0.003 +0.003 +0.034 +0.021
28 0.444* 0.229 0.386* O77 0.655* 0.406 0.026* 0.028 0.871* 0.569
+0.033 +0.021 +0.038 +0.026 +0.030 +0.024 +0.004 +0.003 +0.027 +0.014
38 0.328* 0.118 0.279* 0.095 0.552* 0.319 0.027* 0.027 0.722* 0.454
+0.036 +0.021 +0.034 +0.027 +0.031 +0.017 +0.003 +0.003 +0.034 +0.025
48 0.226* 0.185* 0.484* 0.027* 0.649*
+0.032 +0.027 +0.029 +0.003 +0.034
68 0.144* 0.115* 0.413* 0.024* 0.553*
+0.024 +0.031 +0.024 +0.002 +0.024
98 0.083* 0.075* 0.328* 0.023* 0.386*
+0.019 +0.015 +0.027 +0.002 +0.023

material are stored in different parts of the body in different
proportions. When the snails are exposed to starvation, all
of these stored food materials exhibit a tendency to decrease
with time. During the early periods of starvation, the rate
of decrease is slower when compared to the later periods
in both species (Figures 1-3; Tables 3-5).

In Cerithidea cingulata, the greatest decrease was found
for carbohydrates (89.75% for content and 82.87% for
level) and glycogen (87.94% for content and 79.79% for
level) of the GDG complex. The same trend was noticed
in the GDG complex of Cerithium coralium (77.86% for
content and 68.36% for level of carbohydrates; 76.70% for
content and 66.67% for level of glycogen) but the changes
were less. This was followed by lipids (66.69% for content
and 44.44% for level) in Cerithidea cingulata, whereas in
Cerithium coralium proteins were utilized (54.30% for con-
tent and 34.48% for level) next to carbohydrates. The
protein utilization in Cerzthidea cingulata was found to be
less (63.99% for content and 39.93% for level) when com-
pared to carbohydrates and lipids. In Cerithium coralium,
lipids played a minor role (51.18% for content and 25.89%
for level).

The biochemical constituents of the foot are utilized next
to those of the GDG complex in both species. In the foot
also, the carbohydrates (68.33% for content and 53.95%
for level in Cerithidea cingulata and 57.61% for content
and 50.83% for level in Cerithium coralium) played the
major role as a fuel for energy needs during starvation.
The same trend of utilizing lipids (60.87% for content and

44.12% for level) next to carbohydrates was noticed in
Cerithidea cingulata. Cerithium coralium utilized proteins
(36.86% for content and 25.71% for level) next to carbo-
hydrates. In Cerizthidea cingulata, proteins were least uti-
lized (53.30% for content and 32.88% for level) whereas
lipid utilization was found to be less (43.42% for content
and 22.50% for level) in Cerithium coralium.

The viscera of both animals play almost a minor role
during starvation stress. The biochemical constituents were
reduced on exposure to starvation but to a lesser extent.
In this tissue also, the utilization of carbohydrates (57.70%
for content and 43.54% for level in Cerithidea cingulata
and 52.41% for content and 41.94% for level in Cerzthium
coralium) and glycogen (58.90% for content and 45.16%
for level in Cerithidea cingulata and 51.36% for content
and 40.70% for level in Cerizthtum coralium) was more when
compared to proteins and lipids. Lipid utilization, which
followed that of carbohydrates in Cerithidea cingulata was
57.24% for content and 42.85% for level. In Cerithium
coralium, protein utilization was high (48.17% for content
and 36.17% for level) when compared to lipids. The bio-
chemical constituents that were least affected in Cerzthidea
cingulata and Cerithium coralium were proteins (56.35%
for content and 41.67% for level) and lipids (43.56% for
content and 31.07% for level) respectively.

The levels and contents of different body biochemical
constituents suggest that total carbohydrates constitute the
major fuel during starvation in both species and that, among
all the body components, the GDG complex contributes

Y. Prabhakara Rao et al., 1987

Page 181

Table 5

Effect of starvation on the content of different biochemical constituents in the viscera of Cerithidea cingulata (a) and
Cerithium coralium (b). All values are expressed as g/100 g dry weight of the tissue + SD except TNPS (m mol/100 g
dry weight of the tissue + SD). F-test, * P < 0.05.

No Carbohydrates Glycogen Proteins TNPS Lipids
days a b a b a b a b a b
0 0.825 0.582 0.696 0.403 2.424 1.993 0.023 0.021 1139) 1.313
+0.028 +0.038 +0.039 +0.019 +0.084 +0.056 +0.007 +0.007 +0.045 +0.052
7 0.788 0.538 0.662 0.377 2.308 1.840 0.030* 0.026 1.105 1.435

+0.022 +0.032 +0.011 +0.042 +0.071 +0.064 +0.008 +0.005 +0.049 +0.060

14 0.748 0.495 0.636 0.354 2.163 1.684 0.036* 0.030 1.036 1.294
+0.021 +0.036 +0.032 +0.023 +0.059 +0.050 +0.007 +0.006 +0.043 +0.059

21 0.710 0.443* 0.606 0.323* 2.057* 1.546 0.043* 0.035 0.971* 1.081*
+0.016 +0.044 +0.031 +0.018 +0.052 +0.053 +0.008 +0.006 +0.052 +0.058

28 0.616* 0.385* 0.519 0.284* HO 2.9% 1.342 0.055* 0.040 0.886* 0.961*
+0.026 +0.038 +0.036 +0.025 +0.076 +0.054 +0.007 +0.006 +0.046 +0.042

38 0.588* ODE 0.494* 0.196* 1.699* 1.033 0.055* 0.043 0.795* 0.741*
+0.020 +0.042 +0.040 +0.031 +0.059 +0.042 +0.005 +0.005 +0.049 +0.054

48 0.524* 0.443* 1.471* 0.059* 0.695*
+0.019 +0.038 +0.062 +0.006 +0.057

68 0.455* 0.382* 1.306* 0.058* 0.582*
+0.023 +0.014 +0.064 +0.007 +0.059

98 0.349* 0.286* 1.058* 0.055* 0.487*
+0.038 +0.029 +0.042 +0.006 +0.046

more to meeting energy demands. Thus it is clear from
our results on both species that the decrease in the per-
centage of different biochemical constituents is more when
calculated on the basis of content than on the level. Lipids
are preferred after carbohydrates by Cerithidea cingulata
while Cerithium coralium takes proteins after carbohy-
drates. Finally, proteins and lipids are least utilized by
Cerithidea cingulata and Cerithium coralium in all three
body components. Therefore, the metabolism of both the
cerithiids is ““carbohydrate-oriented” when exposed to star-
vation. Such a condition of carbohydrate-oriented metab-
olism was reported in the cerithiid Clypeomorus clypeo-
morus (MANMADHA Rao, 1977), and several other mollusks
were also found to show “polysaccharide-oriented” me-
tabolism. EMERSON (1967) suggested that certain terres-
trial and freshwater mollusks show carbohydrate-oriented
metabolism, whereas marine mollusks exhibit “‘lipid-ori-
ented” metabolism. VON BRAND et al. (1957) reported
appreciable utilization of polysaccharides in the freshwater
snail Australorbis glabratus. Mytilus edulis, an estuarine and
marine bivalve (BAYNE, 1973), also exhibited reduced levels
of carbohydrates when exposed to starvation. RAMAMURTI
& SUBRAHMANYAM (1976) noticed carbohydrate metabo-
lism in the terrestrial snail Cryptozona semirugata during
starvation. Planorbis corneus, a freshwater snail, also showed
a carbohydrate-oriented metabolism when subjected to
starvation (EMERSON, 1967). In some of marine snails—
Nucella lamellosa (STICKLE & DUERR, 1970), Thais lapillus
(BAYNE & SCULLARD, 1978), Littorina keenae (EMERSON

& DUERR, 1967), and Morula granulata (UMA DEvi et al.,
1986), lipid-oriented metabolism was reported. The im-
portance of lipids and their utilization in invertebrates was
discussed by GIESE (1966). Thus, there is a preferential
utilization of a particular body reserve during starvation.
The estuarine cerithiids of the present investigation belong
to the category of carbohydrate-oriented metabolism, and
thus tend to resemble freshwater rather than marine mol-
lusks.

Earlier investigations (PRABHAKARA RAO & PRASADA
Rao, 1983b) on these cerithiids revealed utilization of gly-
cogen when exposed to oxygen-free seawater. During re-
production, when there is an energy demand for the pro-
duction of sperm and ova, the cerithiid Clypeomorus
clypeomorus (MANMADHA Rao, 1977) also depends on a
carbohydrate reserve food material. Thus, the cerithiids
show carbohydrate-oriented metabolism whenever energy
is needed for the body. The differences in the utilization
of carbohydrates in both species depend on the quantities
stored inside the body. Cerzthidea cingulata stored greater
amounts of carbohydrates compared to Cerithium coralium.
As long as carbohydrate reserves remain, the animals are
able to survive. Death occurs due to insufficient amounts
of carbohydrates, even though lipids and proteins can sub-
stitute to some extent. A similar observation was recorded
in Planorbis corneus where death occurs due to complete
exhaustion of carbohydrates during starvation exceeding
58 days (EMERSON, 1967). The preference of lipid utili-
zation next to carbohydrates in Cerzthium coralium may be

Page 182

attributed to environmental differences. The storage of
body biochemical reserves were found to be higher in Cer-
ithidea cingulata, which normally faces this type of stress
in the upper reaches of the estuary. As food material is
readily available in the habitat of Cerithium coralium, stor-
age inside the body of the animal is unnecessary.

The rates of oxygen consumption in both species de-
creased gradually with increasing periods of starvation.
The weight-specific oxygen consumption was also observed
to decrease during starvation in both species, but the de-
crease was not so rapid when compared to the decrease in
the rates of oxygen consumption (Table 1). However, sim-
ilar trends of decreases in the rates of oxygen consumption
have been reported in several mollusks when exposed to
starvation: Ancylus fluviatilis (BERG et al., 1958), Lymnaea
stagnalis (DUERR, 1965), Littorina keenae (EMERSON &
DUERR, 1967), Potamopyrgus jenkinsi (LUMBYE & LUMBYE,
1965), Nerita albicilla and Nerita chemaeleon (PRASADA
Rao & JAYA SREE, 1983), Thais lapillus (STICKLE & BAYNE,
1982) and Morula granulata (UMA DEvi et al., 1986). The
intercept values also showed a decreasing trend with star-
vation period in both cerithiid species but the decrease was
greater in Certthidea cingulata than Cerithium coralium. In
M. granulata, a similar tendency of decreasing intercept
values “a” when subjected to starvation was reported (UMA
DEVI et al., 1986). However, STICKLE & BAYNE (1982)
did not find any change in the intercept values of Thais
lapillus during starvation, although according to BAYNE &
SCULLARD (1978), the intercept values showed a decreasing
tendency in 7. Japillus. Our results of the weight-specific
oxygen consumption in both species during starvation cor-
roborates results on M. granulata. However, Nucella la-
mellosa exhibited an increased or constant weight-specific
oxygen consumption (STICKLE & DUERR, 1970; STICKLE,
1971). The decreased rates observed in the present inves-
tigation may be an adaptation of the animals to conserve
stored food.

ACKNOWLEDGMENTS

The authors are thankful to the Head of the Department
of Zoology, Andhra University, for providing the necessary
facilities. V.U.D. and Y.P.R. are grateful to the authorities
of the Council of Scientific & Industrial Research for fi-
nancial assistance.

LITERATURE CITED

Bayne, B. L. 1973. Aspects of the metabolism of Mytilus edulis
during starvation. Neth. Jour. Sea Res. 7:339-410.

BAYNE, B. L. & C. SCULLARD. 1978. Rates of oxygen con-
sumption by Thais (Nucella) lapillus (L.). Jour. Exp. Mar.
Biol. Ecol. 32(1):97-111.

BELISLE, B. W. & W. B. STICKLE. 1978. Seasonal patterns in
the biochemical constituents and body component indexes of
the muricid gastropod Thais haemastoma. Biol. Bull. 155:
259-272.

BeErG, K., J. LuMByE & K. W. OCKLEMANN. 1958. Seasonal

The Veliger, Vol. 30, No. 2

and experimental variations of oxygen consumption of limpet
Ancylus fluviatilis. Jour. Exp. Biol. 35:43-73.

CarroL, N. V., R. W. LONGLEY & J. H. Roe. 1956. The
determination of glycogen in liver and muscle by use of
anthrone reagent. Jour. Biol. Chem. 220:583-593.

DuerR, F. 1965. Some effects of diet on the respiratory rate
of freshwater pulmonate snail Lymnaea palustris. Proc. So.
Dak. Acad. Sci. 44:245.

EMERSON, D. N. 1967. Carbohydrate oriented metabolism of
Planorbis corneus (Mollusca. Planorbidae) during starvation.
Comp. Biochem. Physiol. 22:571-579.

EMERSON, D.N. & F. DUERR. 1967. Some physiological effects
of starvation in the intertidal prosobranch Littorina planaxis
(Philippi 1847). Comp. Biochem. Physiol. 20:45-53.

FOLCH, J., LEES, H. & G. H. SLOANE STANELY. 1957. A simple
method for the isolation and purification of total lipids from
animal tissues. Jour. Biol. Chem. 266:497-509.

GiEsE, A. C. 1966. Lipids in the economy of marine inverte-
brates. Physiol. Rev. 40:244-298.

GiEsE, A. C. & M. A. Hart. 1967. Seasonal changes in the
component indices and chemical composition in Katharina
tunicata. Jour. Exp. Mar. Biol. Ecol. 1:34—46.

HIMMELMAN, J. H. 1978. The reproductive cycle of Katharina
tunicata Wood and its controlling factors. Jour. Exp. Mar.
Biol. Ecol. 31:27-41.

KoralAH, K. & B. S. RAJABAINAIDU. 1973. Starvation stress
on the metabolism of tropical freshwater crab Paratelphusa
hydrodromus (Herbert). Indian Jour. Exp. Biol. 13:180-184.

LAWRENCE, A. L., J. M. LAWRENCE & A. C. GIESE. 1965.
Cyclic variations in the digestive gland and glandular oviduct
of chitons (Mollusca). Science 147:510.

Lowry, O. H., N. J. ROSENBROUGH, A. L. Farr, & R. J.
RANDALL. 1951. Protein measurement with the Folin
Phenol reagent. Jour. Biol. Chem. 193:265-275.

LumByYE, J. & J. LuMBygE. 1965. The oxygen consumption of
Potamopyrgus jenkinsi (Smith). Hydrobiology 25:489-500.

MANMADHA Rao, L. 1977. Studies on some aspects of the
biology of a littoral snail Clypeomorus sp. (Gastropoda: Cer-
ithidae) of the Waltair coast. Doctoral Thesis, Andhra Uni-
versity.

MASTANAMMA, P. & R. RAMAMURTI. 1983. Studies on. the
pattern of utilisation of major organic nutrients during star-
vation in the freshwater mussel Lamellidens marginalis (La-
marck). Indian Science Congress Association. 110 pp.

Moore, S. & W.H.STEIN. 1954. A modified ninhydrin reagent
for the photometric determination of amino acids and related
compounds. Jour. Biol. Chem. 211:907-913.

NAGABHUSHANAM, R. & U. D. DESHPANDE. 1982. Changes in
body component indices in relation to reproductive cycle of
chiton Chiton iatricus. Indian Jour. Mar. Sci. 11:276-277.

PRABHAKARA Rao, Y. 1981. Studies on the respiration of cer-
ithiids. Doctoral Thesis, Andhra University.

PRABHAKARA RAO, Y. & D. G. V. PRASADA Rao. 1981. Survival
of Cerithidea (Cerithideopsilla) cingulata (Gmelin 1790) and
Cerithium coralium Kiener 1841 under anoxia and low sa-
linities. Indian Jour. Zoo. 22:29-34.

PRABHAKARA Rao, Y. & D. G. V. PRASADA Rao. 1983a. Effect
of temperature on the size related metabolism of Cerithidea
(Cerithideopsilla) cingulata and Cerithium coralium. Indian
Jour. Zoo. 24:37-43.

PRABHAKARA Rao, Y. & D. G. V. PRASADA RAO. 1983b. End
products of anaerobic metabolism in Cerithidea (Cerithideop-
silla) cingulata (Gmelin 1790) and Cerzthium coralium Kiener
1841. Can. Jour. Zool. 61:1304-1310.

PRABHAKARA Rao, Y. & D. G. V. PRASADA RAO. 1983c. Effect

Y. Prabhakara Rao et al., 1987

of temperature on aquatic and aerial oxygen consumption
of Cerithidea (Cerithideopsilla) cingulata (Gmelin 1790) and
Cerithium coralium Kiener 1841. Monitre Zool. Ital. 17:113-
119.

PRABHAKARA RAO, Y. & D. G. V. PRASADA RAo. 1983d. Aerial
respiration of Cerithidea (Cerithideopsilla) cingulata (Gmelin
1790) and Cerithium coralium Kiener 1841 in relation to
body weight. Proc. Indian Acad. Sci. 92(5):381-386.

PRABHAKARA Rao, Y. & D. G. V. PRASADA Rao. 1984a. Oxy-
gen consumption as a function of salinity in Cerzthidea (Cer-
ithideopsilla) cingulata (Gmelin 1790) and Cerithium coralium
Kiener 1841. Geobios 11:179-182.

PRABHAKARA RAO, Y. & D. G. V. PRASADA RAO. 1984b. Effect
of body size on the respiration of Cerithidea (Cerithideopsilla)
cingulata (Gmelin 1790) and Cerithium coralium Kiener 1841.
Jour. Moll. Stud. 50:92-95.

PRASADA Rao, D. G. V. & P. JAYA SREE. 1983. Effect of
starvation on the oxygen consumption of the intertidal gas-
tropods Nerita albicilla and Nerita chamaeleon. Geobios 10:
276-278.

RAMAMURTI, R. & D. V. SUBRAHMANYAM. 1976. Organic com-
position of haemolymph, hepatopancreas and foot muscle of
garden snail Cryptozona semirugata (Beck) with reference to
starvation. Indian Jour. Exp. Biol. 14:492-498.

Page 183

SNEDECOR, G. W. & W. G. COCHRAN. 1967. Statistical meth-
ods. The Iowa State University Press: Ames, Iowa. 587 pp.

STICKLE, W. B. 1971. The metabolic effects of starving Thais
lamellosa immediately after spawning. Comp. Biochem.
Physiol. 40A:627-634.

STICKLE, W. B. 1975. The reproductive physiology of the in-
tertidal prosobranch Thais lamellosa Gmelin. II. Seasonal
changes in the biochemical composition. Biol. Bull. 148:448-
460.

STICKLE, W. B. & B. L. BAYNE. 1982. Effects of temperature
and salinity on oxygen consumption and nitrogen excretion
in Thais lapillus (L.). Jour. Exp. Mar. Biol. Ecol. 58:1-17.

STICKLE, W. B. & F.G. DuERR. 1970. Effect of starvation on
the respiration and major stores of Thais lamellosa. Comp.
Biochem. Physiol. 33:689-695.

Uma DEvI, V.,Y. PRABHAKARA RAO & D. G. V. PRasaDA Rao.
1986. Starvation as a stress factor influencing the metab-
olism of a tropical gastropod Morula granulata (Duclos).
Proc. Indian Acad. Sci. 95:539-547.

VON BRAND, T., P. MCMAHON & M. O. NOLAN. 1957. Phys-
iological observations on starvation and desiccation of the
snail Australorbis glabratus. Biol. Bull. 113:99-102.

The Veliger 30(2):184-189 (October 1, 1987)

THE VELIGER
© CMS, Inc., 1987

A New and Polytypic Species of Helminthoglypta

(Gastropoda: Pulmonata) from the

Transverse Ranges, California

BARRY ROTH

Research Associate, Department of Invertebrate Zoology, Santa Barbara Museum of Natural History,
Santa Barbara, California 93105, U.S.A.

Abstract. A new species of land snail, Helminthoglypta (Helminthoglypta) salviae, is described from
the Transverse Ranges in southern Kern and northern Ventura counties, California. Two subspecies,
differing in shell sculpture and details of coiling, are recognized, H. salviae salviae from Quatal and
Apache canyons, and H. salviae mina from the vicinity of Frazier Park.

INTRODUCTION

The following species was first recognized as new by the
late W. O. Gregg in the course of his extensive work on
the land snails of southern California. Between 1947 and
1957 he and W. B. Miller collected it at several localities
east and west of the town of Frazier Park, Kern County.
Still earlier, probably some time in the 1930s, George
Willett collected a sample of the same taxon near the head
of San Emigdio Canyon, Kern County. In April 1984, T.
A. Pearce found similar specimens at lower elevations a
short distance to the southwest, in Quatal and Apache
canyons, Ventura County.

The species remained undescribed because anatomical
material was lacking. Species of Helminthoglypta can be
assigned to subgenus only on the basis of genital anatomy
(MILLER, 1985). In April 1986, W. B. Miller, F. G. Hoch-
berg, P. H. Scott, and I secured adequate material for
dissection and the species is described below.

Two subspecies are recognized, differing consistently in
shell characters but identical in genital anatomy. The basic
description below pertains to the species in the broad sense;
it is followed by shorter, differential diagnoses and des-
ignations of type material for each subspecies and a dis-
cussion that again pertains to the species in the broad sense.

The following abbreviations are used: ANSP, Academy
of Natural Sciences of Philadelphia; BR, author’s collec-
tion, San Francisco, California; CAS, California Academy
of Sciences; FMNH, Field Museum of Natural History;
LACM, Natural History Museum of Los Angeles County;
RLR, collection of R. L. Reeder, Tulsa, Oklahoma;

SBMNH, Santa Barbara Museum of Natural History;
TAP, collection of T. A. Pearce, Berkeley, California;
USNM, U.S. National Museum of Natural History;
WBM, collection of W. B. Miller, Tucson, Arizona.

SYSTEMATICS
Family HELMINTHOGLYPTIDAE Pilsbry, 1939
Helminthoglypta Ancey, 1887

Type species: Helix tudiculata A. Binney, 1843, by original
designation.

Subgenus Helminthoglypta s.s.

Helminthoglypta (Helminthoglypta) salviae
Roth, sp. nov.

(Figures 1-8)

Diagnosis of the species: A small Helminthoglypta (Hel-
minthoglypta) with depressed, matte to glossy, umbilicate,
tightly coiled shell, sculptured with minute, slightly wavy,
incised spiral striation. Lip thickened but barely turned
outward. Dart sac moderately small; common duct of mu-
cus bulbs thick-walled; lower chamber of penis short, con-
ical.

Description of the species: Shell small for the genus,
tightly coiled, moderately thin, glossy (in subspecies H. s.
mina) or matte to silky (in subspecies H. s. salviae), de-
pressed, umbilicate, umbilicus contained about 5.3-7.5 (in
H. s. mina) or 6.8-10.5 (in H. s. salviae) times in diameter.

B. Roth, 1987

Page 185

Explanation of Figures 1 to 6

Figures 1-3. Helminthoglypta salviae salviae, shell; holotype
SBMNH 34872, top, apertural, and basal views. Diameter 16.2
mm.

Spire low to very low-conic, whorl profile low-convex,
suture moderately impressed. Embryonic whorls 1.75, set
off from teleoconch by a constriction; initially smooth,
thereafter with weak, irregular wrinkles radiating from
suture, more or less broken up into closely spaced granules
on first whorl, and stronger, widely spaced, diagonally
arranged, round papillae. Early teleoconch whorls with
low, narrow, closely spaced growth rugae (in Hs. saluzae,
some rugae broken up into rows of axially elongated gran-
ules) and, from about middle or end of fourth whorl on,
a system of closely but irregularly spaced, minute, slightly
wavy, incised spiral striae. Striation strongest on shoulder
of whorl behind lip, but also continuing over base into
umbilical region. Base glossy (to matte in H. s. salviae),
inflated, tumid around umbilicus. Last % whorl gently
descending, not constricted behind lip. Aperture broadly
auricular, moderately oblique, peristome at angle of 30°
to vertical; lip narrowly, crudely thickened and turned
outward but barely reflected except at the columellar in-
sertion. Upper limb of peristome produced and slightly
downturned. Inner lip barely encroaching on umbilicus.
Parietal callus thin, its surface granular. Shell pinkish tan
under a yellowish brown periostracum; with a 0.5-mm
wide russet spiral band on shoulder (prolonging trajectory

Figures 4-6. Helminthoglypta saluiae mina, shell; holotype
SBMNH 34876, top, apertural, and basal views. Diameter 15.6
mm.

of suture), with traces of paler zones of equal width on
either side of the band.

Two subspecies are recognized. The holotype of the
nominate subspecies, next presented, is of course the ho-
lotype of the species as well.

Helminthoglypta (Helminthoglypta) salviae salviae
Roth, subsp. nov.

(Figures 1-3, 7)

Diagnosis: Shell matte to silky, umbilicus contained 6.8-
10.5 times in diameter. Early teleoconch whorls with coarse
growth rugae, some rugae broken up into rows of axially
elongated granules. Closely but irregularly spaced, minute,
slightly wavy, incised spiral striae present from end of
fourth whorl on. Base glossy to matte.

Dimensions of holotype: Diameter (exclusive of expand-
ed lip) 16.2 mm, height 8.6 mm, diameter of umbilicus
2.2 mm; whorls 5.25.

Type material: Holotype: Santa Barbara Museum of
Natural History, SBMNH 34872 (shell and dissected soft
anatomy), CALIFORNIA: Ventura County: south side of
Apache Canyon, 4.0 km west-southwest of Nettle Spring

Page 186

10mm

The Veliger, Vol. 30, No. 2

Explanation of Figures 7 and 8

Helminthoglypta salviae, dissections of reproductive system drawn
from projections of stained whole mounts.

Figure 7. H. salviae salviae, paratype SBMNH 34874.

Figure 8. H. saluiae mina, holotype SBMNH 34876; upper part
of uterus and prostate removed.

Campground and 10.4 km east of California State High-
way 33 [NE% sec. 16, T. 8 N, R. 23 W, San Bernardino
Base and Meridian], elevation 1280 m; under pine dead-
falls and dead yuccas. W. B. Miller, F. G. Hochberg, P.
H. Scott, and B. Roth coll., 22 April 1986.

Paratypes: SBMNH 34873 (10 shells and soft parts),
SBMNH 34874 (whole mount of stained genitalia), all
from same locality as holotype. Additional paratypes de-
posited in ANSP, BR, CAS, FMNH, LACM, RLR,
USNM, and WBM.

Referred material: Additional specimens have been ex-
amined from the following localities (all, CALIFORNIA:
Ventura County): Gully entering north side of Quatal
Canyon [NW% sec. 22, T. 9 N, R. 23 W], elevation 1400-
1450 m; under dead yuccas and under rocks. T. A. Pearce
et al. coll., 19 April 1984 (TAP). South side of Quatal
Canyon [NE% SE% sec. 33, T. 9 N, R. 23 WI). T. A.

Abbreviations: ag, albumen gland; as, atrial sac; ds, dart sac; ec,
epiphallic caecum; ep, epiphallus; go, genital orifice; hd, her-
maphroditic duct; mb, mucus gland bulbs; mg, mucus gland mem-
branes; ot, ovotestis; ov, oviduct; pe, penis; pr, penial retractor
muscle; pt, prostate; sd, spermathecal duct; sp, spermatheca; sv,
spermathecal diverticulum; ut, uterus; va, vagina; vd, vas def-
erens.

Pearce coll., 19 April 1984 (TAP). North side of Apache
Canyon, approximately 4.5 mi [7.2 km] west of Nettle
Spring Campground, 0.1 mi from road; under dead yuccas.
F. G. Hochberg coll., 22 April 1986 (SBMNH). Ap-
proximately 0.8 km east of Nettle Spring, Apache Canyon
[NE% sec. 11, T. 8 N, R. 23 W], elevation 1400-1450 m;
under dead yuccas. T. A. Pearce coll., 20 April 1984 (TAP).

Etymology: From the Latin salvia, sage, for the Thistle
Sage (Salvia carduacea Benth.) prominent around the type
locality.

Helminthoglypta (Helminthoglypta) saluiae mina
Roth, subsp. nov.
(Figures 4-6, 8)

Diagnosis: Shell glossy, umbilicus contained 5.3-7.5 times
in diameter. Early teleoconch whorls with fine growth

B. Roth, 1987

Page 187

Table 1

Shell dimensions (in mm) and ratios in Helminthoglypta salviae. Statistics are range, with mean + one SD in parentheses.
Only adult shells included.

Subspecies n D H W H/D U/D

H.s. saluiae 22 14.2-18.9 8.2-10.5 1.5-2.5 5.2-5.6 0.531-0.620 0.095-0.146
(15.83 + 1.18) (OM =EN0'66) = (E925 0!26)) (G:36F = 0:13) > (580) 101024)) > (O12 1! 0/013)

H. s. mina 60 12.3-20.1 6.3-11.0 1.9-3.0 4.8-5.8 0.493-0.570 0.135-0.186
(15.40 + 1.93) (8.24 + 1.06) (2.46+0.25) (5.27 40.24) (0.535 + 0.018) (0.161 + 0.013)

rugae, not broken up into rows of axially elongated gran-
ules. Closely but irregularly spaced, minute, slightly wavy,
incised spiral striae present from about middle of fourth
whorl on. Base glossy.

Dimensions of holotype: Diameter (exclusive of expand-
ed lip) 15.6 mm, height 8.6 mm, diameter of umbilicus
2.4 mm; whorls 5.4.

Type material: Holotype: Santa Barbara Museum of
Natural History, SBMNH 34876 (shell, whole mount of
mantle tissue, and whole mount of stained genitalia), CAL-
IFORNIA: Kern County: 6.1 km west of Frazier Park post
office, north side of Frazier Mountain Park Road [NW
sec. 33, T. 9 N, R. 20 W, San Bernardino Base and
Meridian], elevation 1600 m; under rocks loosely seated
in soil on south-facing ridge. W. B. Miller, F. G. Hoch-
berg, P. H. Scott, and B. Roth coll., 21 April 1986.

Paratypes: SBMNH 34877 (5 shells), from same lo-
cality as holotype, in abandoned wood rat nest, F. G.
Hochberg coll., 21 April 1986. North side of Cuddy Can-
yon [now Frazier Mountain Park] Road 3.8 mi [6.1 km]
west of Frazier Park, elevation 5000 ft [1500 m]; under
rocks. W. O. Gregg coll., 26 January 1947 (SBMNH
34878), 23 March 1947 (SBMNH 34879), 19 December
1953 (SBMNH 34880). Additional paratypes deposited
in ANSP, BR, CAS, FMNH, LACM, RLR, USNM,
and WBM.

Referred material: Additional specimens have been ex-
amined from the following localities (all, CALIFORNIA: Kern
County). The collectors’ original topographic measure-
ments, usually expressed in miles and feet, have been pre-
served, with metric equivalents added.

Head of San Emigdio Canyon, elev. 6000 ft [1800 ml],
under logs. G. Willett coll. (CAS). (Willett’s original label
states “Head of S. Emigdio Can., Mt. Pinos,” which is
internally inconsistent unless ‘““Mt. Pinos” is construed
loosely.) North side of Cuddy Canyon, 4 mi [6.4 km] west
of Frazier Park School, elevation 5200 ft [1600 m]. W. B.
Miller, W. O. Gregg coll., 2 March 1957 (WBM). North
side of highway, 1.9 mi [3.0 km] west of Frazier Park;
under dead yuccas. W. O. Gregg coll., 1 January 1947
(WBM). Gully north of Cuddy Canyon Road, 1.8 mi [2.9
km] west of Frazier Park, elevation 5000 ft [1500 m]; under
granite rocks and rotten wood debris. W. O. Gregg coll.,
23 March 1947 (WBM). North side of Frazier Mountain

Park Road 1.5 mi [2.4 km] west of Frazier Park; under
dead yuccas. F. G. Hochberg coll., 21 April 1986
(SBMNH). Approximately 1 mi [1.6 km] southeast of
Frazier Park, near big rock slide, elevation approximately
5000 ft [1500 m]; under yuccas. W. O. Gregg coll., 15
February 1948 (WBM). North of highway, 1.3 mi [2.1
km] east of Frazier Park; under dead yuccas. W. O. Gregg
coll., 19 December 1953 (WBM). 1.5 mi [2.4 km] east of
Frazier Park, north of bed of Cuddy Creek; under dead
yuccas. W. B. Miller, F. G. Hochberg, P. H. Scott, and
B. Roth coll., 21 April 1986 (BR, SBMNH, WBM).

Etymology: From the Latin mzna, bare, smooth.

DISCUSSION
Shell Variation

On 82 adult specimens from 17 lots, representing most
of the localities from which Helminthoglypta salviae is
known, the following measurements were taken: maximum
diameter (exclusive of the expanded outer lip) (D); height
parallel to the axis of coiling (H); breadth of the umbilicus
parallel to maximum shell diameter (U); and number of
whorls (W), counted by the method of PILsBRy (1939:xi,
fig. B). Relative height of shell (H/D) and relative um-
bilical width (U/D) were calculated. Ranges, means, and
standard deviations of these variables were calculated for
the two subspecies (Table 1). The complete data are on
deposit in the SBMNH. The variation was examined by
means of principal components analysis (BLACKITH &
REYMENT, 1971) with the BMDP Biomedical Computer
Program (FRANE & JENNRICH, 1981) at the University of
California, Berkeley.

A bivariate plot of relative height (H/D) against relative
umbilical width (U/D) (Figure 9) shows that Helmintho-
glypta s. saluiae tends to have relatively higher shells and
relatively smaller umbilical width. Slopes of the regression
lines for the two subspecies differ significantly from each
other (P < 0.001).

Five principal components were computed; the first three
cumulatively account for 96% (51, 37, and 8% respectively)
of the total variance. Table 2 shows loadings of the entered
variables. The first principal component is largely an
expression of overall size and whorl number; a high score
on this factor indicates a large shell with a high whorl
count. The raw measures of size (H and D) and whorl

Page 188

eu ge :
16—@ “ee y =-0.058x+0.164
e ® r)
@ "e e ) e
e
e e C)

° o

e o

y =-0.125x + I

H/D
Figure 9

Relation between relative height of shell (H/D) and relative
umbilical width (U/D) in 82 adult specimens of Helminthoglypta
salviae. Diamonds, H. s. salviae; circles, H. s. mina; s, group
mean for H. s. salviae; m, group mean for H. s. mina.

number are strongly associated (all pairwise correlations
0.808 or greater). The second principal component ex-
presses umbilical size; a high score indicates a shell with
a large umbilicus, both in absolute terms and relative to
the diameter of the shell. Relative height (H/D) loads
negatively on this factor. Both H/D and U/D load pos-
itively on the third factor; a high score indicates a relatively
high shell with a relatively large umbilicus.

The summary statistics of the scores of the two subspe-
cies on these three factors (Table 3) indicate that specimens
of Helminthoglypta s. saluvae tend to score higher on Factor
1, lower on Factor 2, and moderately lower on Factor 3
than specimens of H. s. mina. The combination of a high
score on Factor 1 and a low score on Factor 2 (signifying
a large, relatively high shell with a relatively small um-
bilicus) is especially characteristic of H. s. salviae.

On Figure 10 the scores of the measured specimens on

Table 2

Factor loadings of variables and eigenvalues of factors in
principal components analysis of shells of Helminthoglypta
salviae. Unrotated factors are principal components.

Vari- Factor Factor Factor Factor Factor
able 1 2 3 4 5
D 0.909 0.351 —0.126 —0.175 —0.054
H 0.982 0.006 0.068 —0.152 0.087
W 0.879 0.268 0.041 0.391 —0.002
U 0.125 0.962 0.223 —0.087 —0.031
H/D 0.328 —0.755 0.566 —0.030 —0.031
U/D —0.597 0.725 0.338 0.025 0.035

Eigen-
value 3.045 DOW 0.507 0.216 0.014

The Veliger, Vol. 30, No. 2

Figure 10

Triaxial plot of scores on first three principal components of 82
adult specimens of Helminthoglypta saluiae, coded as described
in text. Diamonds, H. s. salviae; circles, H. s. mina; Hs, holotype
of H. s. salviae; Hm, holotype of H. s. mina. Each symbol rep-
resents one or more specimens.

the first three principal components are plotted on a triax-
ial graph. Factor scores were coded by adding the quantity
necessary to set the lowest score on each factor to zero; a
specimen’s score on an axis of the graph is its corresponding
coded factor score expressed as a percentage of the sum of
its three coded factor scores. The two subspecies are well
discriminated, with shells of Helminthoglypta s. saluiae
tending to score higher on the first axis and lower on the
second axis than shells of H. s. mina. The spread of both
subspecies along the third axis is similar.

Soft Anatomy

Six specimens of Helminthoglypta s. saluviae and one of
H. s. mina were dissected. The figured reproductive sys-
tems are drawn from stained whole mounts.

Table 3

Summary statistics of factor scores in principal components
analysis of shells of Helminthoglypta salviae.

Factor Factor Factor
Subspecies 1 2 3

H. s. salviae

Mean 0.6742 — 1.2336 —0.1175

Maximum 1.802 0.343 2.391

Minimum —0.136 =DV38 —1.903
H. s. mina

Mean —0.2472 0.4523 0.0431

Maximum 2.101 2.057 3.544

Minimum —1.952 —1.028 —2.382

B. Roth, 1987

The body is slaty gray, the mantle collar light tan. The
mantle over the lung is light tan with black spots covering
about 30-40% of the surface, mostly discrete but somewhat
confluent along the dorsal edge. There is a 1 mm by 3 mm
patch of black pigment immediately behind the dorsal end
of the mantle collar.

The reproductive system (Figures 7, 8) is typical of the
nominate subgenus, with a short atrium. The atrial sac is
about % the length of the vagina and bears a rather small
dart sac at its proximal end. The mucus gland bulbs are
of moderate size, joined by a thick-walled, Y-shaped com-
mon duct that enters the atrial sac at the base of the dart
sac. The duct of the spermatheca is fine, somewhat cav-
ernous at its base, and bears a moderately long divertic-
ulum of greater diameter than the duct itself. The penis
has a short, conical lower chamber and a long, double-
walled upper chamber, leading to an epiphallus of the
same diameter as the penis. The epiphallic caecum (‘‘fla-
gellum”’) is long for the size of the animal.

Remarks

Helminthoglypta salviae is the only species of Helmintho-
glypta thus far found in its immediate area. Helmintho-
glypta (Helminthoglypta) cuyama Hanna & Smith, 1937,
occurs approximately 80 km to the west, in the valley of
the Cuyama River (PILsBRY, 1939) and in Colson Canyon,
Santa Barbara County (WBM, LACM). Helminthoglypta
cuyama is larger (to almost 29 mm diameter), also glossy
and depressed, but has malleate sculpture instead of fine
spiral striation; its peristome is reflected. The mantle over
the lung is very dark, 90% or more covered with black
pigment flecks, almost uniform over the last % whorl but
breaking up into spots behind that. The epiphallic caecum
is shorter than that of H. salviae even though the adult
animal is larger, and the dark sac is larger in diameter
than the atrial sac.

The enigmatic Helminthoglypta cuyamacensis venturensis
(Bartsch, 1916), described from Ventura County but never
subsequently recognized, differs from H. salviae in being
coarsely, densely papillose all over. It seems highly im-
probable that H. c. venturensis is really a subspecies of
Helminthoglypta (Rothelix) cuwyamacensis (Pilsbry, 1895),
but until the species is rediscovered and living material
dissected it cannot be firmly allocated.

To the east the geographically nearest taxon is Hel-
minthoglypta (H.) trasku tejonis Berry, 1930, from rock-
slides in the vicinity of Fort Tejon, Kern County, with a
large, tumid, low-conic shell, reaching a maximum di-
ameter of over 30 mm. Also in the vicinity of Fort Tejon
have been found specimens resembling Helminthoglypta

Page 189

(H.) trasku traskii (Newcomb, 1861), one of which was
figured by PItsBry (1939:fig. 85f). Shells that I have ex-
amined are of about the same shape and size as presumed
topotypic H. traski traskiu from Point Fermin, Los Angeles
County, but the incised spiral sculpture is finer (7 striae/
mm on the last % of the body whorl as compared to 4 or
5 striae/mm on H. traski traski). It is possible that these
specimens represent an eastern occurrence of H. salviae.
If they are H. trasku, then dissected material should show
the rather large subglobular dart sac found in that species.

The range of Helmithoglypta salviae is within Juniper-
Pinyon Woodland (KUCHLER, 1977), characterized by open,
mixed groves of California juniper (Juniperus californica
Carr.) and singleleaf pinyon (Pinus monophylla Torr. &
Frém.), both of which here range from large shrubs to
small trees. Yucca whipple: Torr. is locally common, and
the moist interior of its decaying clumps forms prime snail
habitat. East of Frazier Park, H. s. mina was found in
clumps of Y. whipplei in overgrazed pasture. West of Fra-
zier Park, H. s. mina occurs in open areas in an ecotone
between Juniper-Pinyon Woodland and Southern Jeffrey
Pine (Pinus jeffrey: Grev. & Balf.) Forest. We did not find
any Helminthoglypta in pure stands of Jeffrey pine.

ACKNOWLEDGMENTS

I am grateful for the aid and field companionship of Eric
Hochberg and Paul Scott. Tim Pearce kindly put speci-
mens at my disposal. The computer-assisted analysis was
performed with the help of David R. Lindberg and Tim
Pearce. Dick Reeder read and commented on the manu-
script. I especially acknowledge the collaboration of Wal-
ter B. Miller, who collected, dissected, and drew many of
the specimens and identified the Salvia at the type locality
of Helminthoglypta salviae.

LITERATURE CITED

BLACKITH, R. E. & R. A. REYMENT. 1971. Multivariate mor-
phometics. Academic Press: New York.

FRANE, J. & R. JENNRICH. 1981. Factor analysis. Pp. 656-
684. In: W. J. Dixon (ed.), BMDP Biomedical computer
programs. University of California Press: Berkeley.

KUcuHLER, A. W. 1977. The map of the natural vegetation of
California. Pp. 909-939, map. Jn: M. G. Barbour and J.
Major (eds.), Terrestrial vegetation of California. John Wi-
ley and Sons: New York.

MILLER, W. B. 1985. A new subgenus of Helminthoglypta
(Gastropoda: Pulmonata: Helminthoglyptidae). Veliger
28(1):94-98 (1 July 1985).

Pitspry, H. A. 1939. Land Mollusca of North America (north
of Mexico). Acad. Natur. Sci. Philadelphia, Monogr. 3, 1(1):
1-573.

The Veliger 30(2):190-195 (October 1, 1987)

THE VELIGER
© CMS, Inc., 1987

A New Species of Naquetia (Muricidae)
from the Gulf of Aqaba

ANTHONY D’ATTILIO anp CAROLE M. HERTZ

Department of Marine Invertebrates, San Diego Natural History Museum,
P.O. Box 1390, San Diego, California 92112, U.S.A.

Abstract. Naquetia fosteri D’Attilio & Hertz, sp. nov., is described from the Gulf of Aqaba in the
Red Sea; it is compared to N. trigonula (Lamarck, 1816) and N. annandalei (Preston, 1910).

INTRODUCTION

Eight specimens of a Naquetia species were submitted to
the senior author for identification. While referable to
Naquetia, the new species differs from similar species, N.
trigonula (Lamarck, 1816) and N. annandalei (Preston,
1910), in shell characters and distribution. The new species
has been reported only from the Red Sea at the Gulf of
Aqaba.

TAXONOMIC ACCOUNT
Family MuRICIDAE Rafinesque, 1815
Subfamily Muricinae Rafinesque, 1815
Genus Naquetia Jousseaume, 1880

Type species: Murex triqueter Born, 1778, by original des-
ignation.

Naquetia is a genus of non-spinose trivaricate muricids
with noded axial costae, deep anal sulcus, and anteriorly
webbed varical flanges. Both radula and operculum are as
in Muricinae.

Although Naquetia has been considered a subgenus of
Pterynotus Swainson, 1833 (CERNOHORSKY, 1967, 1971;
VOKES, 1968) and Chicoreus Montfort, 1810 (VOKEs, 1974,
1978; HouarT, 1985), it differs from those genera based
on shell morphology (RADWIN & D’ATTILIO, 1976). While

Explanation

Figures 1, 2. Naquetia fosteri sp. nov., holotype (SDNHM 91996),
92.2 x 37.0 mm (protoconch missing). Type locality: Gulf of
Aqaba, off Eilat, Israel. Apertural (Figure 1) and dorsal (Figure
2) views.

Naquetia has the trivaricate nature of the heavier Chicoreus
(type species: Murex ramosus Linné, 1758), it lacks the
foliaceous varical spines of Chicoreus. In Naquetia the var-
ical extensions are sparse, appearing on the anterior end
of the body whorl and canal. In Pterynotus (type species:
Murex pinnatus Swainson, 1822) the three varical exten-
sions are bladelike flanges that continue over the entire
body whorl and spire.

Naquetia fosteri D’Attilio & Hertz, sp. nov.
(Figures 1-6)

Type material and locality: SDNHM 91996: Holotype
(Figures 1, 2). 92.2 x 37.0 mm. Gulf of Aqaba, off Eilat,
Red Sea.

SDNHM 91997: Paratype (Figures 3, 4). 71.5 x 26.2
mm. Gulf of Aqaba, off Eilat, Red Sea.

SDNHM 91998: Paratype. 75 x 29 mm. Gulf of Aqa-
ba, off Eilat, Red Sea.

Donald Pisor Collection: Paratype (ex Aryeh Hadar
and A. D’Attilio Collections). 77.5 x 30.5 mm. Eilat,
Israel. [Figured in RADWIN & D’ATTILIO, 1976: pl. 15,
fig. 10, as N. annandale.]

Kay Vaught Collection No. 4583: Paratype. 75.7 x 26.5
mm. Off Eilat, Israel. 40-45 m. Dani Bloome, Jeg.

Glass and Foster Collection No. 86-037: Paratype.
94.5 x 36 mm. Eilat, Israel, Dec. 1985.

of Figures 1 to 4

Figures 3, 4. Naquetia fosteri, paratype (SDNHM 91997),
71.5 xX 26.2 mm. Gulf of Aqaba, off Eilat, Israel in 40 m.
Apertural (Figure 3) and dorsal (Figure 4) views.

Page 192

ie Pili ae Se

, j \
mv Ay t DL, == .de

RR aS ect Hib) pew ; ht 5

™ ( on) i Da +--+ ai ite
wh rT cl \

“ay Waza PTT hud -
Anau i,
of 6

Explanation of Figures 5 and 6

Figure 5. Naquetia fosteri, paratype (Glass and Foster Collec-
tion). Camera lucida drawing of protoconch, x 20.4.

Figure 6. Naquetia fosteri, detail of sculpture at edge of apertural
flange, <2.5.

Glass and Foster Collection No. 85-1045: Paratype.
93 x 37 mm. Eilat, Israel.

Glass and Foster Collection: Paratype. 81 x 30 mm.
Gulf of Aqaba, Red Sea.

Etymology: It is with great pleasure that we name this
species for Robert Foster, who with Charles Glass has
been generous in making specimens from their collections
available both for study and as additions to the malacology
collection of the San Diego Natural History Museum.

Description: Shell (Figures 1-4) large (to 94.5 x 36 mm),
moderately fusiform with 7-8 convex postnuclear whorls
and protoconch of 142 convex nuclear whorls (Figure 5).
Spire relatively low, less than one-half shell length. Suture
impressed; aperture narrow, lenticular—ovate; outer lip edge
strongly erect and recurved, with 14 denticles becoming
lirae extending into aperture; anal sulcus well defined,
narrow, deep, V-shaped; inner lip mostly appressed; canal
long, sinuous, narrowly open, weakly recurved distally;
siphonal fasciole retaining two prior canal terminations.
Three prominent rounded varices extending to and

The Veliger, Vol. 30, No. 2

Figure 7

Naquetia annandale: (Preston, 1910), apertural view of holotype
(ZSI Reg’d. nom. 4708/1), 76.5 mm long (per Preston). Type
locality: ““Off Gopalpore,” Bay of Bengal.

abutting previous whorls; varices appearing with first post-
nuclear whorl; receding side of varix weakly concave; 3-
5 intervarical costae, irregularly distributed. Fluted varical
flanges on lower portion of body whorl extend to canal.

Body-whorl sculpture of 10 primary spiral cords, 2 of
which are above shoulder, with 3 additional, widely spaced
cords on canal. Transverse cords with minor interstitial
cords throughout, most defined on canal portion of flange.
Raised nodes formed where transverse cords cross costae;
growth striae very weakly defined (Figure 6). First 5 tel-
eoconch whorls vary from bright pink to pale light orange,
with cream-colored varices; remaining 3 whorls rich pink,
cream, and brown; sometimes with faint indications of 3
darker brownish bands on body whorl. (In the holotype
the color has faded to pale orange.) Aperture white.

Distribution: Naquetia fosteri is known only from the area
off Eilat, Israel, in the northern end of the Gulf of Aqaba.

Remarks: Although Naquetia fosteri is related morpho-
logically to its congeners N. annandale: (Preston, 1910)
(Figure 7) and N. trigonula (Lamarck, 1816), material
examined confirms that N. fosteri is a distinct taxon (see
Table 1). Thirteen specimens of N. annandale: from 48.2
to 104.9 mm in height and 8 specimens of N. fosteri from
71.5 to 94.5 in height were examined. Naquetia annandalei
is broader than N. foster. The protoconch of N. annandalei
consists of 32 rounded (Figure 8) rather than 1% rounded
whorls as in N. fosteri (Figure 5). The outer lip of N.
annandalei is crenulate lacking lirae within, whereas that
of N. fosteri bears 14 denticles which become lirate inte-

A. D’Attilio & C. M. Hertz, 1987

Page 193

Wy SORES ate oan

riorly. Naquetia annandalei has 8 moderately convex post-
nuclear whorls and the body whorl is encircled by 14
extremely fine nodose spiral cords which form knobs as
they cross the costae. The entire shell is transversely, mi-
croscopically sculptured, giving the shell a sandpaper-like
texture (Figure 9). Naquetia fosteri, with 7 to 8 postnuclear
whorls, has 10 strong primary cords with minor interstitial
cords and no microsculpture.

Naquetia trigonula (Figure 10) is a smaller species, at-
taining a height of 55.5 mm compared to 94.5 mm for N.
fosteri. Naquetia trigonula has a protoconch of 2%4-2%
tabulate whorls (Figure 11) contrasted to the 1% rounded
whorls in N. fosteri. In the 30 specimens of N. trigonula
studied, the teleoconch is of 5 to 6 rapidly expanding whorls
with 1 or 2 strongly noded intervarical costae and a body
whorl of 10 rows of knobby spiral cords with fine inter-
stitial cords and extremely fine granular microsculpture.

Explanation of Figures 8 and 9

Figure 8. Naquetia annandalei (Preston, 1910). Camera lucida
drawing of protoconch of specimen (SDNHM 81673), 65.0 mm
long, showing three rounded whorls. Shaded area designates
missing portion, x 20.4.

Figure 9. Naquetia annandalei, detail of spiral sculpture on body
whorl, X7.7.

Table 1

Comparison of shell morphology in Naquetia fosteri sp. nov., N. annandale: and N. trigonula.

Protoconch
Teleoconch
Maximum height
Spire-height-to-total-

height ratio, mean*
Maximum width on

body whorl
Width-height ratio

(W/H), mean
Aperture

Outer lip

Spiral sculpture

Axial sculpture

N. fosteri

1% convex whorls
7-8 whorls

94.5 mm

0.385

35 mm
0.384

lenticular-ovate; deep, narrow
anal sulcus with one node on
columellar side of sulcus

14 denticles becoming lirate
within

10 strong primary cords on
body whorl and canal with
minor interstitial cords; no
microsculpture

trivaricate, 3 or 4 noded inter-
varical costae

N. annandalei

3% rounded whorls
8 whorls

104.9 mm

0.322

46 mm
0.419

ovate with deep V-shaped anal
sulcus; two nodes on apertur-
al side of sulcus with thick-
ened ridge on columellar side

crenulate, no lirae within

14 nodose cords on body whorl
and canal, with fine nodose
interstitial cords; extremely
fine granular microsculpture

trivaricate, 3 or 4 intervarical
costae, often only distin-
guished by nodes at the
shoulder

* Measured from receding side of apertural varix to tip of spire.

N. trigonula

2%-2% tabulate whorls
5-6 whorls

55.5 mm

0.385

19.5 mm
0.434

lenticular with V-shaped anal
sulcus; one node on columellar
side of sulcus

13 or 14 denticles becoming lirate
within

10 nodose cords on body whorl
with fine nodose interstitial
cords; extremely fine granular
microsculpture

trivaricate, 1 or 2 strongly noded
intervarical costae

Page 194 The Veliger, Vol. 30, No. 2

Figure 10

Naquetia trigonula (Lamarck, 1816) (SDNHM 87737), 49.3 mm
long, apertural view.

Naquetia fosteri, with 7 to 8 postnuclear whorls, lacks
microsculpture and bears 3 or 4 noded intervarical costae.

Naquetia trigonula occurs throughout the Indo-Pacific
and N. annandale: is found from the Bay of Bengal to the
Philippine Islands and southeastern Japan; N. fosterz is

known only in the northern end of the Gulf of Aqaba. TCE TTT AT eC FTN
{ty Sf 5 t

\
> = <
X SS sy BS
N S

Yee

ACKNOWLEDGMENTS

Diarra

The following friends and colleagues have placed speci-
mens at our disposal: Charles Glass and Robert Foster,

Explanation of Figures 11 to 13

Figure 11. Naquetia trigonula (Lamarck, 1816), 55.5 mm long
(SDNHM 85974). Camera lucida drawings showing four views
of the protoconch, x 20.4.

Figures 12, 13. Naquetia trigonula, 55.5 mm long (SDNHM
80840). Camera lucida drawings of transverse sculpture of spiral
cords with depressed areas containing microsculpture. Figure 12.
Spiral cords, x2.5. Figure 13. Detail of microsculpture in in-
terspaces, <7.7.

A. D’Attilio & C. M. Hertz, 1987

both of Santa Barbara, California, donated the holotype
(SDNHM 91996) and one paratype (SDNHM 91998)
and specimens of other Naquetia species. Marion Magee
of Speedway, Indiana, donated a paratype (SDNHM
91997). Donald Pisor of San Diego, California, Kay Vaught
of Scottsdale, Arizona, and Eugenia Wright of Phoenix,
Arizona, lent paratype specimens. N. V. Subba Rao of the
Zoological Survey of India kindly provided photographs
of the type of N. annandale:. William K. Emerson and
Emily H. Vokes gave helpful suggestions, and Eugene
Coan critically reviewed the manuscript. Theo Fusby typed
the preliminary and final drafts.

Unless otherwise noted, the photography is by David
K. Mulliner.

LITERATURE CITED

Born, I. [Edler von]. 1778. Index rerum naturalium Musei
Caesarei Vindobonensis, pars I. Testacea. [Verzeichniss der
naturlichen Seltenheiten des k. k. naturalien Kabinets zu
Wien, erster Theil. Schalthiere.]. Pp. [xlii] + 458 + [80] +
[2]; 1 pl. [not seen] Vindobonae (Krausiana).

CERNOHORSKY, W.O. 1967. The Muricidae of Fiji (Mollusca:
Gastropoda). Pt. 1. Subfamilies Muricinae and Tritonali-
inae. Veliger 10(2):111-132, pls. 14 and 15 (Oct. 1).

CERNOHORSKY, W. O. 1971. Contribution to the taxonomy of
the Muricidae (Gastropoda: Prosobranchia). Veliger 14(2):
187-191 (Jan. 1).

Page 195

HouartT, R. 1985. Gros plan sur les Naquetia (Gastropoda:
Muricidae). Xenophora 29:8-14 (Sept.—Oct.).

JOUSSEAUME, F. P. 1880. Divison methodique de la famille de
Purpurides. Le Naturaliste, yr. 2(42):335-336 (Dec. 15).

LAMaRCK, J.B. P.A.DEM.bDE. 1816. Tableau encyclopédique
et méthodique detrois régnes de la nature (vers. testaces).
Pls. 315-448. Paris.

Montrort, P. D. DE. 1810. Conchyliologie systematic, et clas-
sification méthodique des coquilles 2:676 pp. Paris.

PRESTON, H. B. 1910. Descriptions of new shells. Rec. Indian
Mus., Calcutta 5:118-119, fig. 3.

RaApDwin, G. E. & A. D’ATTILIO. 1976. Murex shells of the
world. Stanford Univ. Press: Stanford, California. 284 pp.,
32 pls., 192+ text figs.

RAFINESQUE, C. S. 1815. Analyse de la nature ou tableau de
universe et des corps organisés. Pp. 5-6, 136-149, 218-223.
Varravecchea: Palermo.

SwAINson, W. 1833. Zool. Illus. 2(3):22, pl. 100. Mollusca.
London.

VoKEs, E. H. 1968. On the identity of Murex trigonulus of
authors (Gastropoda: Muricidae). Jour. Conchol. 26(5):300-
304, pl. 13. (Oct.).

Vokes, E. H. 1974. On the identity of Murex triqueter Born
(Gastropoda: Muricidae). Veliger 16(3):258-264, 1 pl. (Jan.
1).

VoKEs, E. H. 1978. Muricidae (Mollusca: Gastropoda) from
the eastern coast of Africa. Ann. Natal Mus. 23(2):375-418,
pl. 5 (Oct.).

The Veliger 30(2):196-205 (October 1, 1987)

THE VELIGER
© CMS, Inc., 1987

Pyropeltidae, a New Family of Cocculiniform

Limpets from Hydrothermal Vents

by

JAMES H. McLEAN

Los Angeles County Museum of Natural History,
Los Angeles, California 90007, U.S.A.

AND

GERHARD HASZPRUNAR

Institut fur Zoologie, Universitat Innsbruck,
Technikerstr. 25, A-6020 Innsbruck, Austria

Abstract.

A new genus, Pyropelta, is proposed for two new species from hydrothermal vents: the

types species, P. musaica, from the Juan de Fuca Ridge off Washington, and P. corymba, from the
Guaymas Basin in the Gulf of California. Shells resemble some genera of Pseudococculinidae in having
a similar pattern of erosion. Absence of cephalic lappets, differences in the excretory system, presence
of an osphradium, and major differences in the radula warrant recognition of the new family Pyropeltidae
for the genus. Relationships of the Pyropeltidae among the Lepetellacea are discussed, with comparisons
to those families with a similar radula (Pseudococculinidae, Osteopeltidae). The two species live directly
on sulfide crust, unlike all other Lepetellacea, which are usually associated with biogenic substrata.

INTRODUCTION

The hydrothermal-event environment has yielded a num-
ber of remarkable discoveries among mollusks. Although
limpets of a number of families are well represented
(McLEAN, 1985b), the presence of cocculiniform limpets
in the hydrothermal-vent habitat had not been recognized
until now. In a preliminary report on limpets of the hy-
drothermal vents, MCLEAN (1985b) noted the absence of
members of this group, a generalization that is here emend-
ed. Large numbers of one new species described here were
first collected at the Juan de Fuca Ridge by the submersible
Pisces IV in July 1986. A single specimen of a species from
the Guaymas Basin had been collected in January 1982,
but its radula was not examined and its affinity not as-
certained until now.

The cocculiniform limpets include the families Coccu-
linidae Dall, 1881; Lepetellidae Dall, 1882; Addisoniidae
Dall, 1882; Bathysciadiidae Dautzenberg & Fischer, 1900;
Cocculinellidae Moskalev, 1971; Bethyphytophilidae
Moskalev, 1978; Pseudococculinidae Hickman, 1983; and
Osteopeltidae Marshall, in press. One family with coiled

shells has been recognized, the Choristellidae Bouchet &
Waren, 1979. These families have recently received new
attention, starting with papers by MOSKALEv (1971, 1973,
1976, 1978) and followed by HICKMAN (1983) who gave
the first SEM illustrations of radulae, and papers by
1986) and McLEAN (1985a).
HASZPRUNAR (1987, in press a, b, c, d) has anatomical

MARSHALL (1983,

studies underway relating to these families.

In this paper another cocculiniform family is described.
It has a distinctive radular plan and unique combinations
of anatomical characters, and it does not require a substrate
of biological origin. Other families of cocculiniform limpets
occur and feed upon a variety of substrates including wood
or other plant material, polychaete tubes, bone, cephalopod

beaks, crab exoskeletons, and elasmobranch egg cases.

Type material is placed in the Los Angeles County
Museum of Natural History (LACM), the Museum Na-
tional d’Histoire Naturelle, Paris (NMNH), the National
Museum of Natural History, Washington, D.C. (USNM),
and the National Museum of New Zealand, Wellington

(NMNZ).

J. H. McLean & G. Haszprunar, 1987

TAXONOMY
Superfamily LEPETELLACEA

Limpets with horseshoe-shaped muscle, lacking juvenile
coiling, or coiled with a single (left) shell muscle (Cho-
ristellidae only). With or without oral lappets and epi-
podial tentacles. Several secondary gill-leaflets (pallial and/
or subpallial). Heart monotocardian. Two kidneys, the left
one small or vestigial and usually connected with the pe-
ricardium, the right one larger and isolated. Limpet fam-
ilies hermaphroditic with separated, ventral testis, and dor-
sal ovary; right cephalic tentacle often serving as copulatory
organ, never with copulatory verge proper; open or closed
seminal groove at right neck; gonoduct(s) without glands.
Statocysts with several or many cones. Rachidian tooth of
radula well developed.

PYROPELTIDAE McLean & Haszprunar, fam. nov.

Because a single genus in this new family is presently
known, the generic description and discussion serve for
that of the family.

Pyropelta McLean & Haszprunar, gen. nov.
Type species: Pyropelta musaica sp. nov.

Diagnosis: Shell small for superfamily (maximum length
4.6 mm), white, periostracum unknown (probably worn
off). Apex central, at highest elevation of shell. Protoconch
and exterior sculpture eroded. Exterior surface of shell
etched with irregular concentric lines reflecting uneven
erosional pattern. Shell margin thin, fragile. Shell interior
with pattern of concentric, wavy, alternating light and dark
reflective areas, a pattern not corresponding to the exterior
pattern of irregular concentric lines. Muscle scar closer to
mid-point of shell than to margin; anterior tips of scar
broadly inflated, tips projecting inward. Muscle scar con-
tinuous anteriorly with pallial attachment scar, which to-
gether with muscle scar makes a continuous oval scar.
Surface central to scar areas thickened, opaque white. In-
terior muscle scar pattern visible externally through trans-
lucent shell.

Radula. Rachidian tooth broad, with rounded lateral
extremities, tapered base, and long, tapered neck, with
small overhanging tip. Shaft and base of first lateral broad,
inner edge excavated to accommodate base of rachidian,
upper portion of shaft tapering to long overhanging cutting
area. Second and third laterals largest, similar, each with
pronounced elbow on outer side and deeply grooved upper
arm of shaft for accommodation of adjacent teeth; cutting
area long, serrated, tip rounded. Fourth lateral unlike first
three, shaft broad, lacking elbow, its cutting area concavely
arched and serrate on inner side. Fifth lateral similar to
fourth in having broad shaft and undulating cutting edge,
its tip with projecting cusps. Lateromarginal plate elongate
(visible from basal side of ribbon), positioned between tooth
rows. Marginal basal plate present; marginals numerous,

Page 197

not separated at base, first and second marginal not en-
larged.

External! anatomy. Oral disc broad, circular, lappets lack-
ing; cephalic tentacles equal, like the mantle devoid of
papillae. No subpallial glands. Foot with deeply contracted
central area. Posterior pair of epipodial tentacles present.
Gill tips especially prominent on right side; mantle skirt
above neck thin. Right cephalic tentacle (copulatory organ)
simple and solid; from its base an open seminal groove
leads to the genital opening along right neck.

Internal anatomy. Two uninterrupted shell muscles
forming a horseshoe-shaped organ, the left muscle slightly
larger than right. Pedal gland small but distinct. Mantle
cavity shallow, from left (in dorsal view) a distinct os-
phradium, pericardium, left kidney, anus, right excretory /
genital opening, and genital gland. No hypobranchial gland.
Secondary gill leaflets up to 18, at central and/or right
pallial roof, continuing into right subpallial cavity. Gill
leaflets respiratory and provided with sensory pockets.
Heart monotocardian, pericardium large, ventricle pos-
terior to auricle. Left kidney extremely small and vestigial
(max. dimension 100 x 60 xX 30 um), isolated. Right
kidney forms large coelomic system; fused with single and
simply ciliated gonoduct immediately at common opening.
Testis ventral, ovary dorsal, more posterior, separated, no
accessory glands or vesicles along common gonoduct. Eggs
large and yolk-rich, no allosperm observed. From excre-
tory/genital opening a glandular open duct runs forwards
to anterior end of right shell muscle, further continued by
seminal groove. Jaws paired, consisting of toothlike ele-
ments. Sublingual cavity shallow, no subradular organ.
Two pairs of cartilages, posterior pair smaller, radular
diverticulum present. Salivary glands paired, pouchlike.
Anterior oesophagus broad, with dorsal food channel and
pouches. Folds of channel posteriorly fused during oesoph-
ageal torsion. Stomach with gastric shield and tooth, lack-
ing protostyle, with paired mid-gut glands, the right en-
larged anteriorly. Several intestinal loops, rectum
penetrating ventricle. Nervous system streptoneurous, hy-
poathroid, with pedal ganglia (two commissures), visceral
ganglia indistinct; a single (left) osphradial ganglion. No
eyes or optic nerve; osphradial epithelium well developed;
statocysts with several statocones.

Remarks: Two species are known, the type species from
hydrothermal vents on the Juan de Fuca Ridge off Wash-
ington, and Pyropelta corymba from hydrothermal vents
in the Guaymas Basin, Gulf of California. Pyropelta is
the only hydrothermal vent limpet not known from either
of the two sites on the East Pacific Rise (near 21 N and
13 N), where 14 limpet species are known from each site
(MCLEAN, 1985b).

Exterior surfaces of both species are eroded, but this is
probably normal for the genus. It is compensated by thick-
ening of the shell from within. Such erosion also takes
place in other deep-sea habitats and is usual in many
pseudococculinid species.

Page 198

The Veliger, Vol. 30, No. 2

Explanation of Figures 1 to 4

Figures 1 to 4. SEM views of radula of Pyropelta musaica sp.
nov. Lateral teeth numbered 1 through 5; 6 = lateromarginal
plate; 7 = marginal basal plate.

Figure 1. Rachidian, laterals, and marginals. Bar = 20 wm.

Pyropelta musaica McLean & Haszprunar, sp. nov.

(Figures 1-8, 9A)

Description: Shell (Figures 5, 7, 8) small (maximum length
4.6 mm), white, periostracum unknown (probably eroded).
Height low to moderate, that of holotype 0.26 times length.
Apex central, at highest elevation of shell. Protoconch and
exterior sculpture entirely eroded. Exterior surface of shell
etched with irregular concentric lines reflecting uneven
erosional pattern. Shell margin thin, fragile; plane of ap-
erture nearly flat in shells of oval outline; laterally com-
pressed forms have ends raised relative to sides. Muscle
scar pattern visible from exterior through translucent shell;

Figure 2. Basal view, showing rachidian, laterals, lateromarginal
plate, and marginal basal plate. Bar = 20 um.
Figure 3. Rachidian and laterals. Bar = 10 um.

Figure 4. Laterals 1, 2, and 3. Bar = 4 um.

muscle closer to mid-point of shell than to margin; anterior
tips of scar broadly inflated, tips projecting inward. Shell
interior with pattern of concentric, wavy, light and dark
reflective areas, not corresponding to exterior pattern of
irregular concentric lines. Shell thin and transparent enough
to reveal the exterior pattern from inner side. Muscle scar
of interior as described above, continuous anteriorly with
pallial attachment scar, which together with muscle scar
makes a continuous oval scar. Surface central to scar areas
thickened, opaque white.

Dimensions. Length 3.0, width 2.7, height 1.0 mm (ho-
lotype).

Radula (Figures 1-4) described above under generic
heading.

J. H. McLean & G. Haszprunar, 1987

Page 199

Explanation of Figures 5 to 8

Figures 5 to 8. Pyropelta musaica.
Figure 5. Holotype. Exterior, interior (anterior at top), and lat-
eral (left side) views of shell. Length 3.0 mm.

Figure 6. Holotype body out of shell, dorsal and lateral (right
side) views, showing gill lamellae projecting on right. For ori-
entation see Figure 9A. Length 1.9 mm.

Figure 7. Ventral view of paratype showing light and dark re-
flective areas of shell interior. Length 3.2 mm.

Figure 8. Ventral and dorsal views of paratype (laterally com-
pressed form). Length 3.1 mm.

Page 200

»

sm

The Veliger, Vol. 30, No. 2

a?

Figure 9

Comparison of arrangement of gill-leaflets in Pyropelta species. Dorsal view, schematic. A. P. musaica. B. P.
corymba. Abbreviations: gl, gill leaflets; mc, posterior end of mantle cavity; pc, pericardium; r, rectum; sm, shell

muscle.

External anatomy (Figures 6-8, 9A) described under
generic heading.

Internal anatomy described under generic heading. For
purposes of comparison with Pyropelta corymba, the left
kidney of P. musaica is extremely small (30 x 50 x 30
um). Gill leaflets up to 25 wm long at right pallial roof,
reaching posteriorly in right subpallial cavity up to two-
thirds of body length (Figure 9A). Anterior edge of shell
muscles not specialized.

Type locality: Axial Seamount, Juan de Fuca Ridge, off
Washington (45°59.5'N, 130°03.5’'W), 1575 m.

Type material: Holotype and paratypes from 6 Pisces IV
dives, July-August 1986, depth and coordinates as above.
Holotype from dive 1733, paratypes from following dives:
6 specimens, dive 1723, Hammond’s Hell Vent, 19 July;
10 specimens, dive 1728, Southern Axial Vent, 29 July;
16 specimens, dive 1729, Anemone Ridge, 30 July; 8 spec-
imens, dive 1730, Eastern Axial, 31 July; 1 specimen, dive
1731, Post Taylor’s Vent, 1 August; 50 specimens, dive
1733, Not-so-miserable Vent, 3 August. Holotype, LACM
2275 (dive 1733); 65 paratypes LACM 2276; 10 paratypes
USNM 784760, 10 paratypes MNHN; 5 paratypes
NMNGZ. Specimens from dive 1733 were sectioned.

Etymology: The name is Latin for mosaic, with reference
to both the exterior erosional pattern and the interior band-
ing pattern.

Remarks: In addition to radular differences, Pyropelta
musaica may be distinguished from pseudococculinid
species on its generic characters—the pattern of light and

dark banding on the shell interior, and the lack of oral
lappets. Although the shell is variable in height, the most
elevated specimens are not as high as the single specimen
of P. corymba sp. nov.

There is a considerable range of expression in apertural
shape, ranging from broadly oval (Figure 5) to laterally
compressed, with more elevated ends (Figure 8). Some
shells, as for example the holotype (Figure 5), change
during growth from somewhat compressed to lower and
more oval. This range of variation in apertural shape
suggests that individuals are adapted to a habitual site of
attachment, which they may leave in foraging for food.

General descriptions of the biota at Axial Seamount (the
type locality) are given by CHASE et al. (1985) and TUNNI-
CLIFFE et al. (1985), although the existence of Pyropelta
musaica is not mentioned, as it had not been collected
prior to 1986. According to V. Tunnicliffe (personal com-
munication), these limpets live “in the warm water vents
and on surrounding rocks.” They were apparently not
collected directly from washings of the vestimentiferan tubes.
The species has not been found at the Explorer Ridge
farther to the north. One other much larger limpet (de-
scription by MCLEAN, in press) is common at all sites on
the Juan de Fuca and Explorer ridges.

Pyropelta corymba McLean & Haszprunar, sp. nov.

(Figures 9B, 10, 11)

Description: Shell (Figure 10) small (maximum length
3.0 mm), white, periostracum lacking. Elevation extremely
high, that of holotype 0.83 times length. Apex posterior,

J. H. McLean & G. Haszprunar, 1987

Page 201

Explanation of Figures 10 and 11

Figures 10 and 11. Pyropelta corymba sp. nov. Holotype.

Figure 10. Exterior, interior (anterior at top), and lateral (left
side) views of shell. Length 3.0 mm.

at highest point of shell, two-thirds shell length from an-
terior margin. Protoconch and exterior sculpture eroded,
no evidence of sculpture on exterior surface. Exterior sur-
face of shell etched with irregular concentric lines reflecting
uneven erosional pattern. Shell margin thin, easily broken;
plane of aperture with ends raised relative to sides. Shell
interior with pattern of concentric, wavy alternating light
and dark reflective areas, not corresponding to the exterior
pattern of irregular concentric lines. Shell thin and trans-
parent enough to reveal the exterior pattern from inner
side. Muscle scar closer to mid-point of shell than to mar-
gin; anterior tips of scar broadly inflated, tips projecting
inward, continuous anteriorly with pallial attachment scar,
which together with muscle scar makes a continuous oval
scar. Surface central to scar areas thickened, opaque white.
Muscle scar pattern apparent on exterior of shell.

Figure 11. Ventral (in shell) and lateral views of body (left side)
prior to sectioning. For orientation see Figure 9B.

Dimensions. Length 3.0, width 2.5, height 2.5 mm (ho-
lotype).

Radula not available (specimen sectioned).

External anatomy (Figure 11) as described for the genus.

Internal anatomy as described for the genus. For com-
parison with Pyropelta musaica, the left kidney of P.
corymba is larger (100 x 60 x 40 um). Gill leaflets up
to 60 um long, extending from central pallial roof to the
right, reaching posteriorly in right subpallial cavity up to
one-half body length (Figure 9B). Anterior edge of shell
muscles bordered by a strongly ciliated epithelial ridge.

Type locality: Southern trough of Guaymas Basin, Gulf
of California, off Guaymas, Sonora, Mexico (27°01.0'N,
111°25.0'W), 2022 m.

Type material: 1 specimen from type locality, Alvin dive

Page 202

The Veliger, Vol. 30, No. 2

Figure 12

Comparison of coelomic systems of lepetellacean families. A. Lepetellidae. B. Osteopeltidae, Cocculinellidae, and
Addisoniidae. C. Pyropeltidae. D. Pseudococculinidae. Abbreviations: gd, gonoduct; lk, left kidney; od, oviduct; pc,
pericardium; r, rectum; rc, releasing chamber; rk, right kidney; vd, vas deferens.

1176, 19 January 1982. Holotype, LACM 2277. No other
specimens are known. The body of the holotype has been
sectioned.

Etymology: The name is derived from Greek, corymbos,
peak, with reference to the high profile of the shell.

Remarks: The shell meets the generic criteria for Pyro-
pelta in being relatively small, with exterior erosion as
well as the interior pattern of alternating light and dark
reflective areas. It differs from P. musaica in having a
much higher profile and a more posterior apex. The left
kidney is larger, the gill leaflets are longer, and the anterior
edge of the shell muscle is bordered by a strongly ciliated
epithelial ridge (unspecialized in P. musaica).

Although the height of the single specimen places it well
outside the range of variation noted in Pyropelta musaica,
it is impossible to tell in the absence of additional material
whether this specimen represents the extreme or the norm.

One other limpet (described by MCLEAN, in press) is
known from the Guaymas Basin site. A general description
of the hydrothermal site and its biota was given by
LONSDALE (1984).

This species has previously been cited (MCLEAN 1985b:

160, 162) under the vernacular name “Group-C, high-
conical.” There is no affinity to other Group-C limpets
(terminology of HICKMAN, 1983) for which the descrip-
tions are now in preparation by McLean, the anatomy
under study by V. Fretter. The lack of cephalic lappets
led to that assignment, but the radula and anatomy were
not examined at that time.

DISCUSSION
Systematic Position

The shell and anatomy of Pyropelta fall well within
the lepetellacean “bauplan” (see above definition of su-
perfamily). Affinity is closest to the Pseudococculinidae
and Osteopeltidae on the basis of similarities in the shell,
radula, and gill leaflets. The erosional pattern of the shell
and corresponding prominence of the muscle scar occurs
in typical species of the Pseudococculinidae. Except for the
lack of cephalic lappets and the lack of papillae on the
cephalic tentacles and mantle margin (both also absent in
Osteopelta Marshall, in press), the features of the external
anatomy also agree with what is known of pseudococcu-
linids.

J. H. McLean & G. Haszprunar, 1987

The internal anatomy of Pyropelta also resembles that
of the Pseudococculinidae. However, all characters in com-
mon are regarded as primitive (plesiomorphic) for the
Lepetellacea (HASZPRUNAR, in press d), including the pres-
ence of sensory pockets at the efferent axes of the gill-
leaflets (such pockets also occur in the Lepetellidae; un-
published observation of G.H. on three species in two
genera).

Differences from the Pseudococculinidae are found es-
pecially in the excretory system. The Pseudococculinidae,
as well as other lepetellacean families so far investigated,
have a small, but distinct left kidney, which communicates
with the pericardium (Figure 12D). In contrast, the left
kidney of Pyropelta is extremely small, vestigial, and iso-
lated (Figure 12C). This reduction resembles that of the
Fissurellacea (ANDREWS, 1981, 1985). The reasons for
these reductions are unknown in either family.

In contrast, the relation between the right kidney and
the genital system is the same in Pyropelta and in the
Pseudococculinidae. In both families the right kidney is
fused with the genital duct immediately at the common
opening (Figures 12C, D). The condition is more derived
than that in the Lepetellidae, in which the distal portions
of the right kidney and the distal genital duct form a
releasing chamber that differs in histology from both or-
gans (Figure 12A). The final condition among the Le-
petellacea is represented by Osteopelta Marshall, in press,
Cocculinella Thiele, 1909, and Addisonia Dall, 1882
(HASZPRUNAR, 1987, in press b, d). There the common
gonoduct is separated into vas deferens and oviduct, and
three independent openings exist (Figure 12B). Thus, Py-
ropelta and the Pseudococculinidae represent an inter-
mediate state with respect to coelomic conditions. Similar
trends (common distal releasing chamber or duct—com-
mon opening—separate openings, male and female ducts)
also occur among the Bivalvia (MACKIE, 1984).

There are major differences between the radula of Py-
ropelta and that of pseudococculinids. Pyropelta agrees
with the pseudococculinid plan in having a broadly inflated
rachidian and the first lateral has the broad shaft and elbow
characteristic of pseudococculinids. As in the Pseudococ-
culinidae (and unlike the Cocculinidae), the lateromar-
ginal plate and marginal basal plate are present. It differs
from the general plan in having long overhanging cutting
areas on the first three pairs of laterals. The fourth lateral
of Pyropelta is an independent element that more closely
resembles the fifth, outer lateral; in pseudococculinids the
fourth lateral is similar to the second and third laterals
and has a pronounced elbow. Marginal teeth of Pyropelta
also differ; inner marginals, particularly the second pair,
are not enlarged as in some pseudococculinids. In some
pseudococculinid genera, the enlarged cusps of the second
pair of marginals make them the largest and most poten-
tially functional teeth; in Pyropelta, the three inner lat-
erals are the most effective teeth in the row.

The osteopeltid radula differs from both the pseudo-

Page 203

cocculinid and pyropeltid radula in lacking marginal basal
plates (see MARSHALL, in press). As in the Pseudococcu-
linidae, the osteopeltid radula has a massive fifth lateral.
It is unique in having a massive first lateral.

The alimentary tract of Pyropelta strongly resembles
that of the Pseudococculinidae, being primitive for the
superfamily (HASZPRUNAR, in press c). The only difference
is the presence of two mid-gut glands, whereas only one
exists in the Pseudococculinidae. Osteopelta differs in its
specialized buccal apparatus (a single pair of cartilages
only) and in having distinct oesophageal glands instead of
pouches.

Most features of the nervous system of Pyropelta, as
well as the Pseudococculinidae, reflect primitive lepetel-
lacean conditions, whereas Osteopelta has a concentrated
cerebropedal ring (HASZPRUNAR, in press a). Like Coc-
culinella the pedal cords of Pyropelta are concentrated and
represent true ganglia with only two commissures. As is
typical for lepetellacean limpets, there is a single (left)
osphradial ganglion. However, Pyropelta still has retained
an osphradial epithelium, whereas the Pseudococculinidae
generally lack it. Otherwise the sense organs (lack of eyes,
a single posterior pair of epipodial tentacles, lack of sub-
radular organ, statocysts with several statoconia) are typ-
ical for the Lepetellacea. The presence of oral lappets is
regarded as primitive for cocculiniform limpets and for
archaeogastropods in general (HASZPRUNAR, in press d).
Among the Lepetellacea, these lappets are lost in certain
Lepetellidae (MOSKALEV, 1978) and in the derived lepe-
tellacean families Osteopeltidae, Cocculinellidae, and Ad-
disoniidae (HASZPRUNAR, 1987, in press b, d).

Summing up, Pyropelta is obviously closely related to
the Pseudococculinidae. However, the lack of cephalic lap-
pets, and the absence of sensory papillae on the cephalic
tentacles and mantle margin, the major differences in the
radula, the vestigial left kidney, the existence of pedal
ganglia, and a distinct osphradial epithelium warrant the
recognition of the new family Pyropeltidae. Moreover, the
condition of the right excretory/genital system places the
family closest to the Pseudococculinidae (shell muscles sol-
id, right kidney forming a large coelomic system), but at
present it cannot be decided which family first split off.
The Lepetellidae (still with muscle bundles, releasing
chamber, small and compact right kidney) are clearly more
primitive than both, whereas the remaining lepetellacean
families Osteopeltidae, Cocculinellidae, Addisoniidae, and
Choristellidae, with distinct oesophageal glands and com-
pletely separated gonoducts, are more highly derived than
Pyropelta and the Pseudococculinidae (HASZPRUNAR, in
press d). Thus, the sequential (sensu WILEY, 1981) ar-
rangement of lepetellacean families is now as follows: Le-
petellidae, Pseudococculinidae, Pyropeltidae, Osteopelti-
dae, Cocculinellidae, Addisoniidae, and Choristellidae; the
poorly known Bathyphytophilidae may belong here. The
Cocculinidae and Bathysciadiidae together comprise the
Cocculinacea (HASZPRUNAR, in press a).

Page 204

Biology and Evolutionary History

Pyropelta appears to be unique among cocculiniform
limpets in living directly on a non-biological substrate—
the sulfide crust deposits of deep-sea hydrothermal vents.
Other cocculiniform limpets live and feed on such sub-
strates as wood, cephalopod beaks, whale or fish bone, and
elasmobranch egg cases. The hydrothermal-vent habitat
has an abundant food source in the chemoautotrophic bac-
teria that proliferate on surfaces exposed to vent water.
This food source would not require the specialization nec-
essary for feeding on the harder substrates utilized by other
members of the suborder, although such substrates may
be weakened by bacterial activity.

It could be argued that the unspecialized feeding of
Pyropelta reflects the basal biology of the Lepetellacea
and Cocculinacea. This view is supported by the pyropeltid
radula, which seems more primitive than that of the pseu-
dococculinids in having functional lateral teeth (the long
overhanging cutting edges, contrasting with the small, hook-
shaped cutting edges of pseudococculinids) and unspe-
cialized marginal teeth. Also, the remaining alimentary
tract of Pyropelta is primitive for lepetellaceans, but this
is less significant, considering that certain pseudococculin-
ids with specialized feeding (e.g., Tentaoculus neolithodicola
on carapaces of deep-sea stone crabs, MARSHALL, 1986)
also have a primitive alimentary tract (HASZPRUNAR, in
press c).

However, considering that Pseudococculinidae, the most
primitive family of Lepetellacea, and Cocculinidae, the
most primitive family of Cocculinacea, feed predominantly
on wood, wood-feeding was probably basic to cocculini-
form evolution (HASZPRUNAR, in press d). Moreover, the
lack of oral lappets, a derived condition, favors the sec-
ondary nature of the feeding biology of Pyropelta. Thus,
it seems more likely that the hydrothermal-vent habitat
and nourishment of Pyropelta are secondary for the Le-
petellacea.

Although most other hydrothermal-vent limpets are
probably descendents of shallow-water ancestors (Mc-
LEAN, 1981, 1985b, in press), Pyropelta has its closest
relatives, the Pseudococculinidae, among typically deep-
water to abyssal forms. Of the other mollusks in this hab-
itat, the turrid gastropods and most of the bivalves also
are related to deep-water genera (TURNER e¢ al., 1985).
The hydrothermal-vent habitat has evidently been invaded
by different groups from different habitats at different
times.

ACKNOWLEDGMENTS

We are grateful to those who entrusted the material of the
new species to us for description: Verena Tunnicliffe of
the University of Victoria, British Columbia, and Fred
Grassle of Woods Hole Oceanographic Institution. His-
tologic sections were prepared by B. Ruthensteiner (Vi-
enna). Photographs of the limpet bodies were made by

The Veliger, Vol. 30, No. 2

LACM museum volunteer Bertram C. Draper. SEM mi-
crographs of radulae were made at the Center for Electron
Microscopy and Microanalysis at the University of South-
ern California, with the help of Clif Coney. Bruce Mar-
shall of the National Museum of New Zealand made
helpful comments on the manuscript.

LITERATURE CITED

ANDREWS, E. B. 1981. Osmoregulation and excretion in proso-
branch gastropods. Part 2: Structure in relation to function.
Jour. Moll. Studies 42:199-216.

ANDREWS, E. B. 1985. Structure and function in the excretory
system of archaeogastropods and their significance in the
evolution of gastropods. Phil. Trans. Royal Soc. Lond., ser.
B, 310:383-406.

BoucHET, P. & A. WAREN. 1979. The abyssal molluscan fauna
of the Norwegian Sea and its relation to other faunas. Sarsia
64:212-243.

CHASE, R. L., J. R. DELANEY, J. L. KARSTEN, H. P. JOHNSON,
S. K. JUNIPER, J. E. Lupton, S. D. Scott, V. TUNNICLIFFE,
S. R. HAMMOND & R. E. McDurr. 1985. Hydrothermal
vents on an axis seamount of the Juan de Fuca Ridge. Nature
331:212-214.

HASZPRUNAR, G. 1987. The anatomy of Addisonia (Mollusca,
Gastropoda). Zoomorphology 106:269-278.

HASZPRUNAR, G. In press a. Anatomy and affinities of coccu-
linid limpets (Mollusca, Archaeogastropoda). Zool. Scripta.

HASZPRUNAR, G. In press b. Anatomy and systematic position
of the bone-feeding limpets, Cocculinella minutissima (Smith)
and Osteopelta mirabilis Marshall, 1987. Jour. Moll. Stud.

HASZPRUNAR, G. In press c. Anatomy and affinities of pseu-
dococculinid limpets (Mollusca, Archaeogastropoda). Zool.
Scripta.

HASZPRUNAR, G. In press d. Comparative anatomy of coccu-
liniform gastropods and its bearing on archaeogastropod sys-
tematics. Proc. 9th Int. Malacol. Congr. Edinburgh 1986.

HICKMAN, C.S. 1983. Radular patterns, systematics, diversity,
and ecology of deep-sea limpets. Veliger 26:73-92.

LONSDALE, P. 1984. Hot vents and hydrocarbon seeps in the
Sea of Cortez. Pp. 21-24. In: P. R. Ryan (ed.), Deep-sea
hot springs and cold seeps. Oceanus 7.

MackiE, G. L. 1984. Bivalves. Pp. 351-418. Jn: A. S. Tompa,
N. H. Verdonk & J. A. M. Van Den Biggelaar (eds.), The
Mollusca. Vol. 7. Reproduction. Academic Press: New York.

MaRSHALL, B. A. 1983. The family Cocculinellidae (Mollusca:
Gastropoda) in New Zealand. Rec. Natl. Mus. New Zeal.
2(12):139-143.

MarsHALL, B. A. 1986. Recent and Tertiary Cocculinidae and
Pseudococculinidae (Mollusca: Gastropoda) from New Zea-
land and New South Wales. New Zealand Jour. Zool. 12:
505-546.

MARSHALL, B. A. In press. Osteopeltidae (Mollusca: Gas-
tropoda): a new family of limpets associated with whale bone
in the deep-sea. Jour. Moll. Stud.

MCLEAN, J. H. 1981. The Galapagos Rift limpet Neomphalus:
relevance to understanding the evolution of a major Paleo-
zoic-Mesozoic radiation. Malacologia 21:291-336.

McLean, J. H. 1985a. The archaeogastropod family Addi-
soniidae Dall, 1882: life habit and review of species. Veliger
28(1):99-108.

McLean, J. H. 1985b. Preliminary report on the limpets at
hydrothermal vents. Pp. 159-160. In: M. L. Jones (ed.),

J. H. McLean & G. Haszprunar, 1987

The hydrothermal vents of the eastern Pacific: an overview.
Bull. Biol. Soc. Wash. 6:159-166.

McLgEan, J. H. In press. New archaeogastropod limpets from
hydrothermal vents, superfamily Lepetodrilacea. Part 1: Sys-
tematic descriptions. Phil. Trans. Royal Soc. Lond., ser. B.

MoskaLEv, L. I. 1971. New data on the systematic position of
the gastropod molluscs of the order Cocculinida Thiele, 1908.
Pp. 59-60. Jn: Molluscs, ways, methods and results of their
investigation. Abstracts, Fourth Conference on the Investi-
gation of Molluscs. Academy of Sciences of the USSR, Zoo-
logical Institute. Nauka, Leningrad [in Russian].

MoskKALEV, L. I. 1973. Pacific Ocean Bathysciadiiae (Gas-
tropoda) and related forms. Zoological Journal 52(9):1279-
1303 [in Russian].

MoskaLeEv, L. I. 1976. On the generic classification in Coc-
culinidae (Gastropoda, Prosobranchia). Pp. 59-70. In: Z. A.
Filatova (ed.), Deep water bottom fauna of the Pacific Ocean.
Works of the P. P. Shirshov Institute of Oceanology, The
Academy of Sciences of the USSR 99 [in Russian].

Page 205

Moska.Lev, L. I. 1978. Lepetellidae (Gastropoda, Prosobran-
chia) and related forms. Pp. 132-146. In: The deep-sea
bottom fauna of the subantarctic part of the Pacific Ocean.
Akademiya Nauk SSSR, Trudy Instituta Okeanologii P. P.
Shirshov 113 [in Russian].

TUNNICLIFFE, V., S. K. JUNIPER & M. E. DE BurRGH. 1985.
The hydrothermal vent community on Axial Seamount, Juan
de Fuca Ridge. Pp. 453-464. In: M. L. Jones (ed.), The
hydrothermal vents of the eastern Pacific: an overview. Bull.
Biol. Soc. Wash. 6.

TuRNER, R. D., R. A. LuTz & D. JABLONSKI. 1985. Modes
of molluscan larval development at deep-sea hydrothermal
vents. Pp. 167-184. In: M. L. Jones (ed.), The hydrothermal
vents of the eastern Pacific: an overview. Bull. Biol. Soc.
Wash. 6.

WILEY, E. O. 1981. Phylogenetics, the theory and practice of
phylogenetic systematics. John Wiley: New York. xv + 439

PP.

The Veliger 30(2):206-210 (October 1, 1987)

THE VELIGER
© CMS, Inc., 1987

NOTES, INFORMATION & NEWS

Fact or Artifact?
by
S. van der Spoel
Institute for Taxonomic Zoology,
University of Amsterdam,
Plantage Middenlaan 53,
Amsterdam, The Netherlands

The conclusion by GILMER (1986) that the minute, skinny,
and aberrant developmental stages in pteropods described
by the present author are artifacts is rejected. Though the
function of the developmental stages in the life cycle of
pteropods, their ecology, and phylogenetic development are
not fully understood, such stages exist and can be distin-
guished on the basis of published data (see literature in
GILMER, 1986). Furthermore, living aberrant stages have
already been described (PAFORT-VAN IERSEL, 1985), all of
which induces me to comment on Gilmer’s conclusions
(referring throughout to the 1986 paper). For most liter-
ature references I also refer to GILMER (1986).

In the abstract, Gilmer states (p. 48) that “inaccurate
anatomical observations” were made with regard to de-
velopmental stages, but nowhere in his paper is an accurate
anatomical observation given. The paper deals only with
the external morphology and body weight of complete
living or preserved animals.

The term “aberrant” is considered by Gilmer to cover
also skinny and minute stages. However, I have always
used these three as different terms: all forms that are aber-
rant are not aberrant “stages.” Lumping the terms is enor-
mously confusing, the more so because the skinny and
minute stages are more related to each other than to the
aberrant stage.

Gilmer states (p. 48) that aberrants are unknown from
living specimens. However, they have been described from
living specimens (PAFORT-VAN IERSEL, 1985; PAFORT-VAN
IERSEL & VAN DER SPOEL, 1986), and the skinny or minute
stages are even known as fossils (JANSSEN, 1985).

Gilmer states (p. 51) that I described in 1962 and 1967
food particles from the gut of aberrants; I did not. VAN
DER SPOEL (1967) described food particles from juveniles
and minute stages, but for the aberrant stages it is described
(1962, 1967) that the gut is not completely developed and
without food.

Gilmer states (p. 51) that predation or parasites may
be responsible for the aberrant forms, but I have indicated
that this is not the case (VAN DER SPOEL, 1967:183, 1973:
209).

More importantly, Gilmer studied the external mor-
phology of living and preserved specimens, but nothing is
said about their anatomy and histology. The anatomy and
histology of minute, skinny, and aberrant stages was, how-

ever, fully described (literature in Gilmer) and they differ
from the histology and anatomy of normal specimens. Gil-
mer gives no attention to this difference. Although fixation
and preservation may alter external morphology and even
the (always artificial) histological picture of tissues, they
never alter anatomy, number of cells, types of organs, or
configuration of muscles and ducts. I based the skinny,
minute, and aberrant developmental stages on such struc-
tures.

Preservation affects normal and developmental stages in
a probably comparable way, so it is sometimes impossible
to tell from the external morphology of a specimen in which
stage it is. Aberrants, skinnies, and minutes were originally
described from preserved material and it is evident that
they will have another appearance when alive (cf. GILMER,
1986:fig. 1c; PAFORT-VAN IERSEL & VAN DER SPOEL, 1986).
Only thorough histological and anatomical study, not pro-
vided by Gilmer, can give an answer. Gilmer’s criticisms
made with regard to growth and shell formation in skinny
and minute stages are correct. The mantle indeed has to
be in contact with the shell to secrete it, and some pres-
ervation artifacts were probably misinterpreted by me; in
living minute and skinny stages the mantle can reach the
shell margin.

Gilmer’s fig. 1a pictures a fully developed and living
Clio pyramidata, whereas his fig. 1b shows a normal, pre-
served C. pyramidata not showing the glove-shaped body
form of an aberrant stage. The specimen in fig. 1b is not,
however, the same specimen as that in fig. 1a, although
this is stated. The shell in 1b is broader than in 1a, which
suggests that the two specimens may even have originated
from different populations. Furthermore, the protoconch
is preserved in the fig. 1b specimen after fixation, whereas
it appears missing in the living specimens of fig. 1a. Thus
it seems impossible that 1a and 1b are of the same spec-
imen. These two pictures prove only that fixation alters
body shape, a well known fact.

Gilmer’s fig. 1c shows a young Cuvierina columnella with
the caudal spine intact but without the closing septum
below the teleoconch (this specimen should for this reason
already be considered a skinny specimen). The body, ex-
cept for the mantle gland, is extremely slender further
indicating that this is a skinny stage. Fig. 1d represents a
skinny specimen of C. columnella with all the characters
of this stage; it is probably the same as that in fig. Ic.
These two figures do not support Gilmer’s ideas but rather
my published data. With animals like those photographed
more about shell formation in the skinny stage could have
been studied.

Gilmer’s fig. le shows a not yet full grown Cavolinia
tridentata. Fig. 1f also shows a C. tridentata but not, as is
stated, the same specimen as fig. le, judging from the

Notes, Information & News

Page 207

differences in the shape of the upper lip and lateral spines
and the shell parameters. The specimen in fig. le is likely
in a growth phase between the minute and adult stages,
judging from shell development. However, only a histo-
logical study can prove if it is a minute or not; an external
investigation is not sufficient here.

Finally, that a SCUBA diver does not easily encounter
the skinny, minute and, especially, the aberrant stages in
the relative small volume of water investigated is not as-
tonishing. Such forms are only rarely found in museum
material collected from millions of cubic meters of water.

Literature Cited

GILMER, R. W. 1986. Preservation artifacts and their effects
on the study of euthecosomatous pteropod mollusks. Veliger
29(1):48-52.

JANSSEN, A.W. 1985. Evidence for the occurrence of a “‘skinny”
or “minute stage” in the ontogenetical development of Mio-
cene Vaginella (Gastropoda, Euthecosomata) from the North
Sea and Aquitaine basins. Meded. Werkgr. Tert. Kwart.
Geol. 21(4):193-204.

PAFORT-VAN IERSEL, T. 1985. A contribution to pelagic zoo-
geography of the mid North Atlantic Ocean. Doctoral The-
sis, Univ. of Amsterdam. 185 pp.

PAFORT-VAN IERSEL & S. VAN DER SPOEL. 1986. Schizogamy
in the planktonic opisthobranch Clio—a previously unde-
scribed mode of reproduction in the molluscs. Intern. Jour.
Reprod. Develop. 10:43-50.

VAN DER SPOEL, S. 1962. Aberrant forms of the genus Clio
Linnaeus, 1767 with a review of the genus Proclio Huben-
dick, 1951. Beaufortia 9(107):173-200.

VAN DER SPOEL, S. 1967. Euthecosomata, a group with re-
markable developmental stages (Gastropoda, Pteropoda). J.
Noorduyn & Zn: Gorinchem. 375 pp.

VAN DER SPOEL, S. 1973. Strobilation in a mollusc; the devel-
opment of aberrant stages in Clio pyramidata Linnaeus, 1767
(Gastropoda, Pteropoda). Bijdr. Dierkunde 43(2):202-215,
pls. 1, 2.

Response to “Fact or Artifact?” by
S. van der Spoel
by
Ronald W. Gilmer
Department of Biology,
Woods Hole Oceanographic Institution,
Woods Hole, Massachusetts 02543, U.S.A.

In GILMER (1986) I presented results from a simple ex-
periment using live thecosome pteropods, regardless of the
collection method. Van der Spoel’s objections that the fig.
1 photographs are not of the same individuals are not only
wrong but beside the point, as the figures merely show
results that are easily repeatable. For clarification, all pho-
tographs in fig. 1 of GILMER (1986) are as labeled. The
animal in fig. 1a was swimming when photographed—it
is a ventral view and is slightly tilted; fig. 1b (after pres-
ervation) is a dorsal view in a flat plane so that the pro-
toconch is now apparent.

I consider van der Spoel’s statement (in ‘Fact or Ar-
tifact?”?) that the mantle can reach the shell aperture in
his “minute” and “skinny” stages an admission that he
misrepresented in his published descriptions what he con-
siders to be their live morphology. This is not a trivial
admission as van der Spoel relied heavily on external mor-
phology in establishing these stages. The contracted, con-
torted body and mantle are supposed to be major char-
acteristics of live individuals. Indeed, the “skinny” and
“minute” names of the stages are obviously taken from
the external morphology of preserved specimens. I find no
histological or anatomical evidence from van der Spoel’s
descriptions of these two stages that could not be due to
fixation artifacts.

Recent studies on the aberrant stages of Clio, primarily
by Pafort-van Iersel (cited in “Fact or Artifact?’’), correctly
show the need to separate this phenomenon from the “mi-
nute and skinny” controversy. The apparent morpholog-
ical changes that occur in some specimens of this genus
may represent the first documented case of molluscan re-
production via segmentation and splitting of the body.
Further work is necessary to demonstrate clearly whether
this remarkable phenomenon is not a collection artifact
caused by trauma in the plankton net or not due to parasitic
infection, to which this particular genus is often subjected
(e.g., PERKINS, 1983; GOTTO, 1986).

Literature Cited

GILMER, R. W. 1986. Preservation artifacts and their effects
on the study of euthecosomatous pteropod mollusks. Veliger
29:49-52.

Gotto, R. V. 1986. A new parasitic copepod crustacean of
uncertain affinities: Megallecto thiriott n. gen., n. sp. Bull.
Zool. Mus. Amsterdam 10:185-189.

PERKINS, P.S. 1983. The life history of Cardiodectes medusaeus
(Wilson), a copepod parasite of lanternfishes (Myctophidae).
Jour. Crust. Biol. 3:70-87.

California Malacozoological Society

California Malacozoological Society, Inc., is a non-profit
educational corporation (Articles of Incorporation No.
463389 were filed 6 January 1964 in the office of the
Secretary of State). The Society publishes a scientific quar-
terly, The Veliger. Donations to the Society are used to
pay a part of the production costs and thus to keep the
subscription rate at a minimum. Donors may designate
the Fund to which their contribution is to be credited:
Operating Fund (available for current production); Sav-
ings Fund (available only for specified purposes, such as
publication of especially long and significant papers); or
Endowment Fund (the income from which is available;
the principal is irrevocably dedicated to scientific and
educational purposes). Unassigned donations will be used
according to greatest need.

Contributions to the C.M.S., Inc., are deductible by
donors as provided in section 170 of the Internal Revenue

Page 208

Code (for Federal income tax purposes). Bequests, lega-
cies, gifts, and devises are deductible for Federal estate and
gift tax purposes under sections 2055, 2106, and 2522 of
the Code. Upon request, the Treasurer of the C.M.S., Inc.,
will issue suitable receipts which may be used by donors
to substantiate their tax deductions.

Subscription Rates and Membership Dues

At its regular Annual Business Meeting on 23 September
1986, the Executive Board of the California Malacozoo-
logical Society, Inc., set the subscription rates and mem-
bership dues for Volume 30 of The Veliger. For affiliate
members of the Society, the subscription rate for Volume
30 will be US$25.00; this now includes postage to domestic
addresses. For libraries and nonmembers the subscription
rate will be US$50.00, also now with postage to domestic
addresses included. An additional US$3.50 is required for
all subscriptions sent to foreign addresses, including Can-
ada and Mexico.

Affiliate membership in the California Malacozoologi-
cal Society is open to persons (no institutional member-
ships) interested in any aspect of malacology. There is a
one-time membership fee of US$2.00, after payment of
which, membership is maintained in good standing by the
timely renewal of the subscription.

Send all business correspondence, including subscription
orders, membership applications, payments for them, and
changes of address to C.M.S., Inc., P.O. Box 9977, Berke-
ley, CA 94709.

Page Charges

Although we would like to publish papers without charge,
high costs of publication require that we ask authors to
defray a portion of the cost of publishing their papers in
The Veliger. We wish, however, to avoid possible financial
handicap to younger contributors, or others without fi-
nancial means, and to have charges fall most heavily on
those who can best afford them. Therefore, the following
voluntary charges have been adopted by the Executive
Board of the California Malacozoological Society: $30 per
printed page for authors with grant or institutional support
and $10 per page for authors who must pay from personal
funds (2.5 manuscript pages produce about 1 printed page).
In addition to page charges, authors of papers containing
an extraordinary number of tables and figures should ex-
pect to be billed for these excess tables and figures at cost.
It should be noted that even at the highest rate of $30 per
page the Society is subsidizing well over half of the pub-
lication cost of a paper. However, authors for whom the
regular page charges would present a financial handicap
should so state in a letter accompanying the original manu-
script. The letter will be considered an application to the
Society for a grant to cover necessary publication costs.
We emphasize that these are voluntary page charges and
that they are unrelated to acceptance or rejection of manu-

The Veliger, Vol. 30, No. 2

scripts for The Veliger. Acceptance is entirely on the basis
of merit of the manuscript, and charges are to be paid after
publication of the manuscript, if at all. Because these con-
tributions are voluntary, they may be considered by authors
as tax deductible donations to the Society. Such contri-
butions are necessary, however, for the continued good
financial health of the Society, and thus the continued
publication of The Veliger.

Reprints

While it was hoped at the “birth” of The Veliger that a
modest number of reprints could be supplied to authors
free of charge, this has not yet become possible. Reprints
are supplied to authors at cost, and requests for reprints
should be addressed directly to the authors concerned. The
Society does not maintain stocks of reprints and also cannot
undertake to forward requests for reprints to the author(s)
concerned.

Patronage Groups

Since the inception of The Veliger in 1958, many generous
people, organizations, and institutions have given our jour-
nal substantial support in the form of monetary donations,
either to The Veliger Endowment Fund, The Veliger Op-
erating Fund, or to be used at our discretion. This help
has been instrumental in maintaining the high quality of
the journal, especially in view of the rapidly rising costs
of production.

At a recent Executive Board Meeting, we felt we should
find a way to give much-deserved recognition to those past
and future donors who so evidently have our best interests
at heart. At the same time, we wish to broaden the basis
of financial support for The Veliger, and thus to serve our
purpose of fostering malacological research and publica-
tion. Accordingly, it was decided to publicly honor our
friends and donors. Henceforth, donors of $1000.00 or
more will automatically become known as Patrons of The
Veliger, donors of $500.00 or more will be known as Spon-
sors of The Veliger, and those giving $100.00 or more will
become Benefactors of The Veliger. Lesser donations are
also sincerely encouraged, and those donors will be known
as Friends of The Veliger. To recognize continuing support
from our benefactors, membership in a patronage category
is cumulative, and donors will be listed at the highest
applicable category. As a partial expression of our grati-
tude, the names only of donors in these different categories
will be listed in a regular issue of the journal. Of course,
we will honor the wishes of any donor who would like to
remain anonymous. The Treasurer of the California Mal-
acozoological Society will provide each donor of $10.00 or
more with a receipt that may be used for tax purposes.

We thank all past and future donors for their truly
helpful support and interest in the Society and The Veliger.
Through that support, donors participate directly and im-

Notes, Information & News

portantly in producing a journal of high quality, one of
which we all can be proud.

Donations during 1986-1987
Friends

Dr. Mark Mitchell

Dr. Teuo Miyauti

Dr. J. T. Smith

Dr. Kikutaro Baba

Dr. Alan Bebbington
Dr. K. Ekawa

Mrs. Heidi Petersons
Dr. K. Masuda

Dr. Ellen Moore

Mrs. Gordon Neiswanger
Mr. George R. Plummer
Dr. Ralph T. Smith
Dr. Sakae O’Hara

Mr. Allan Fukuyama
Dr. Carol N. Hopper
A. & S. Miller

Dr. J. J. Landye

Dr. Art L. Metcalf
Dr. Seigoro Takahashi
Dr. Toshiaki Fuse

Dr. R. Tucker Abbott
Dr. E. A. Kay
Anonymous

Mr. John P. McQueen
Dr. Louella R. Saul
Dr. Earl Segal

Mr. Dale V. Stingley
Dr. David R. Lindberg

Benefactors—$100 or more

Mrs. Richard H. Hagemeyer
Dr. Cadet Hand

Dr. Druid Wilson

Dr. A. Richard Palmer

Dr. Frank A. Pitelka

Mr. William Pitt

Dr. Carole S. Hickman

Dr. Howard A. Bern

Dr. John S. Hensill

Dr. Joan Emily Steinberg

Patrons—$1000 or more

Dr. Harold W. Harry
Mrs. Jean M. Cate

Notes to Prospective Authors

The increasing use of computers to prepare manuscript
copy prompts the following notes. We request that the
right margin of submitted papers be prepared “ragged,”

Page 209

that is, not justified. Although right-justified margins on
printed copy sometimes look “neater,” the irregular spac-
ing that results between words makes the reviewer’s, ed-
itor’s, and printer’s tasks more difficult and subject to error.
Similarly, the automatic hyphenation capability of many
machines makes for additional editorial work and potential
confusion; it is best not to hyphenate words at the end of
a line. Above all, manuscripts should be printed with a
printer that yields unambiguous, high-quality copy. With
some printers, especially some of the dot-matrix kinds,
copy is generally difficult to read and, specifically, the
letters “a, p, g, and q” are difficult to distinguish, especially
when underlined as for scientific names; again, errors may
result.

Other reminders are (1) that three copies of everything
(figures, tables, and text) should be submitted to speed the
review process, and (2) absolutely everything should be
double-spaced, including tables, references, and figure leg-
ends.

Because The Veliger is an international journal, we oc-
casionally receive inquiries as to whether papers in lan-
guages other than English are acceptable. Our policy is
that manuscripts must be in English. In addition, authors
whose first language is other than English should seek the
assistance of a colleague who is fluent in English before
submitting a manuscript.

Moving?

If your address is changed it will be important to notify
us of the new address at least six weeks before the effective
date and not less than six weeks before our regular mailing
dates. Send notification to C.M.S., Inc., P.O. Box 9977,
Berkeley, CA 94709.

Because of a number of drastic changes in the regulations
affecting second class mailing, there is now a sizable charge
to us on the returned copies as well as for our remailing
to the new address. We are forced to ask our members and
subscribers for reimbursement of these charges:

change of address and re-mailing of a returned issue—
$5.00.

Sale of C.M.S. Publications

All back volumes still in print, both paper-covered and
cloth-bound, are available only through “The Shell Cab-
inet,’ 12991 Bristow Road, Nokesville, VA 22123. The
same applies to the supplements still in print, with certain
exceptions (see below). Prices of available items may be
obtained by applying to Mr. Morgan Breeden at the above
address.

Volumes 1 through 13, 24, 26, and 27 are out of print.

Supplements still available are: part 1 and part 2, sup-
plement to Volume 3, and supplements to Volumes 7, 11,
14, 15, and 16; these can be purchased from ‘“‘The Shell
Cabinet” only. Copies of the supplement to Volume 17
(“Growth rates, depth preference and ecological succession

Page 210

of some sessile marine invertebrates in Monterey Harbor”
by E. C. Haderlie) may be obtained by applying to Dr.
E. C. Haderlie, U.S. Naval Post-Graduate School, Mon-
terey, CA 93940.

Some out-of-print editions of the publications of C.M.S.
prior to Volume 26 are available as microfiche reproduc-
tions through Mr. Steven J. Long. The microfiches are
available as negative films (printed matter appearing white
on black background), 105 mm xX 148 mm, and can be
supplied immediately. The following is a list of items now
ready:

The Veliger, Vol. 30, No. 2

Volumes 1-6: $9.95 each.

Volumes 7-12: $12.95 each.

Supplement to Volume 6: $3.95; to Volume 18, $6.95.
Send orders to Mr. Steven J. Long, Shells and Sea Life,
1701 Hyland, Bayside, CA 95524.

Single copies of back issues of The Veliger still in print
are available exclusively from:

Conchylien Cabinet,
Grillparzerstrasse 22,
D-6200 Wiesbaden, BRD (West Germany).

The Veliger 30(2):211-212 (October 1, 1987)

THE VELIGER
© CMS, Inc., 1987

BOOKS, PERIODICALS & PAMPHLETS

Living Terebras of the World

by TwiLa BRATCHER & WALTER CERNOHORSKY, edited
by R. TUCKER ABBoTT. 1987. American Malacologists,
Inc.: Melbourne. 240 pp.; 68 pls. + 6 color pls. $54.00.

The systematics of the Terebridae (Neogastropoda) have
been neglected far too long. The evolutionary relationships
within the family remain mysterious; the last comprehen-
sive review is nearly a century old. Terebrid ecology is
also poorly known, despite excellent contributions by B.
A. Miller (1975, Pacific Science 29:227-241; 1979, Pacific
Science 33:289-306) and a few others. Bratcher & Cer-
nohorsky’s volume, although flawed, goes a long way to-
ward summarizing our knowledge of the Terebridae and
correcting two centuries of taxonomic miscues. They have
collaborated to produce a valuable contribution to mal-
acology, worthy of notice by collectors everywhere.

Bratcher & Cernohorsky’s monograph opens with a brief
review of the ecology and life history of terebrid gastropods.
While not comprehensive, the authors do provide a useful
layman’s guide to these ubiquitous marine tropical snails.
There is a brief, and unsatisfying, discussion of the status
of the terebrid genera followed by the centerpiece of their
efforts: a detailed review of each species. Every known
terebrid species (268) is described and illustrated. Com-
plete synonymies are provided for each species and, in
most cases, type specimens are illustrated. The synonymies
appear to be carefully compiled and should go a long way
toward eliminating confusion surrounding terebrid no-
menclature. The geographical range of each species to-
gether with available ecological information is included.
The volume does not include a key to the identification of
species, but species are grouped together by faunal province
and with similar forms to allow quick comparisons. Also,
the authors take reasonable care to identify characteristics
useful for distinguishing similar species.

There is a brief discussion of the fossil record of the
family but the taxonomy of forms known only as fossils is
outside the scope of the present volume. Bratcher & Cer-
nohorsky state that the earliest known terebrid is Eocene
in age, a conclusion at variance with J. D. Taylor et al.
(1980, Palaeontology 23:375-409) who indicate a Late Cre-
taceous (Maastrichtian) origin for the family. Bratcher &
Cernohorsky make no reference to this work, leaving me
to wonder whether they simply overlooked the earlier re-
port or discount it for some unknown reason.

The most serious problem in this volume is the inade-
quate treatment of evolutionary relationships among tere-
brid species. The volume is arguably pre-darwinian. There
is no discussion of, or reference to, evolution within the
family. This might be acceptable in a guide for shell col-
lectors, but not in a taxonomic monograph of an important

clade of prosobranch gastropods. The terebrid genera (and
the authors recognize four: 7erebra Bruguiere, 1789, Has-
tula H. & A. Adams, 1853 [including the subgenera Has-
tula s.s. and Impagnes E. A. Smith, 1873], Duplicaria Dall,
1908, and Terenolla, Iredale, 1929) are avowedly form
genera, without evolutionary significance. The classifica-
tion is entirely conchological. The genus Terebra is em-
ployed explicitly as a taxon of convenience for species
lacking features characteristic of the other genera. These
shortcomings are certainly not of the authors’ making, and
it is one that the authors certainly recognize, but one would
hope to see this longstanding situation resolved or at least
improved. The authors make no attempt to remedy the
inadequacies in terebrid classification. They fail to intro-
duce new information to establish meaningful evolutionary
relationships. But these shortcomings might be one stu-
dent’s treasure trove: Bratcher & Cernohorsky have laid
the groundwork for a excellent study of the evolutionary
relationships of this diverse modern clade. The status of
countless conchological species has been clarified and the
next contribution can move on to include molecular, an-
atomical, shell microstructure or other evidence in a thor-
ough phylogenetic analysis.

The authors are prone to pronouncing judgement with-
out explanation or even acknowledging that different opin-
ions might exist. For example, Rudman (1969, Veliger 12:
53-64) argued that fundamental anatomical differences
exist between species of the genus Pervicacia and the Te-
rebridae. He concluded that the differences indicated the
genus was independently derived from a primitive toxo-
glossan ancestor. Rudman therefore proposed the family
Pervicaciidae as a separate clade of the Toxoglossa. Bratch-
er & Cernohorsky list Rudman’s family as a synonym of
the Terebridae and synonymize Pervicacia with Terebra
but offer no comment, discussion, or justification for these
actions. From the text one would not surmise the existence
of any doubt. In effect, they have casually rejected a le-
gitimate (though not necessarily valid) hypothesis of phy-
logenetic relationships.

Another unfortunate problem with the book is that more
than a few errors have crept into the text. Some are trivial
and can be overlooked, such as occasional failures to ital-
icize binomial names or depths given in odd units (the
depth range of Terebra albida is given as “to 275 mm”
[page 80]: either that depth range is very precisely estab-
lished or else the range extends to 257 m). Others are more
annoying, such as mixing up the numerical sequence of
species’ reference numbers for 11 species, so that the reader
is referred to a particular species number for comparison
but finds that number occupied by a different species. One
wonders how many similar careless errors are to be found
in the synonymies.

Page 212

A separate shortcoming is the disappointing quality of
the black and white plates. Too many illustrations are
fuzzy, lack contrast, or are amateurishly prepared. The
plates are not up to the standards set by other fine pub-
lications of American Malacologists. Nevertheless, collec-
tors will certainly find the numerous illustrations useful
in identifying their shells.

As with most books, one’s estimation of the volume will
follow from one’s expectations. Bratcher & Cernohorsky
have compiled a thorough review of the known terebrid
species, together with detailed summaries of the nomen-
clatural histories of those species. Collectors and malacol-
ogists seeking to identify terebrids or to resolve synonymies
will find the book to be of inestimable value. Others, who
might seek the evolutionary relationships among the species
of Terebridae or between the Terebridae and other tox-
oglossans (assuming the family is a true clade), will find
the volume sadly wanting. The volume is a long overdue
consolidation of our conchological knowledge of the Te-
rebridae. We are now poised to move forward, using mod-
ern techniques and methods of phylogenetic analysis, to
advance and test hypotheses about the taxonomic relation-
ships of terebrid gastropods.

P. W. Signor

The Veliger, Vol. 30, No. 2

A Faunal Study of the Bivalves of San Felipe
and Environs, Gulf of California, from

the Gemmell Collection (1965 to 1976)

by JOYCE GEMMELL, BARBARA W. MYERS & CAROLE M.
HERTZ. 1987. San Diego Shell Club, The Festivus
18(Suppl.):72 pp., 79 text figs. (26 Feb. 1987). Available
for $8.75 domestic postpaid, $9.25 overseas (surface mail)
from the San Diego Shell Club, 3883 Mt. Blackburn Ave.,
San Diego, CA 92111.

This substantial paper is the culmination of several years
of effort by these workers. This, like their earlier papers,
is well illustrated by excellent line drawings, and their
identifications are often based on study of type material.
This is a significant work in the study of the marine bi-
valves of the eastern Pacific, continuing the long tradition
of professional-level contributions by amateurs on the Pa-
cific coast.

Gene Coan

Information for Contributors

Manuscripts

Manuscripts must be typed on white paper, 8/2” by 11”, and double-spaced throughout
(including references, figure legends, footnotes, and tables). If computer generated copy
is to be submitted, margins should be ragged right (1.e., not justified). To facilitate the
review process, manuscripts, including figures, should be submitted in triplicate. The
first mention in the text of the scientific name of a species should be accompanied by the
taxonomic authority, including the year, if possible. Underline scientific names and other
words to be printed in italics. Metric and Celsius units are to be used.

The sequence of manuscript components should be as follows in most cases: title page,
abstract, introduction, materials and methods, results, discussion, acknowledgments, lit-
erature cited, figure legends, figures, footnotes, and tables. The title page should be on a
separate sheet and should include the title, author’s name, and address. The abstract
should describe in the briefest possible way (normally less than 200 words) the scope,
main results, and conclusions of the paper.

Literature cited

References in the text should be given by the name of the author(s) followed by the
date of publication: for one author (Smith, 1951), for two authors (Smith & Jones, 1952),
and for more than two (Smith e¢ al., 1953).

The “literature cited” section must include all (but not additional) references quoted
in the text. References should be listed in alphabetical order and typed on sheets separate
from the text. Each citation must be complete and in the following form:

a) Periodicals
Cate, J. M. 1962. On the identifications of five Pacific Mitra. Veliger 4:132-134.

b) Books

Yonge, C. M. & T. E. Thompson. 1976. Living marine molluscs. Collins: London.
288 pp.

c) Composite works

Feder, H. M. 1980. Asteroidea: the sea stars. Pp. 117-135. In: R. H. Morris, D. P.

Abbott & E. C. Haderlie (eds.), Intertidal invertebrates of California. Stanford Univ.
Press: Stanford, Calif.

Tables
Tables must be numbered and each typed on a separate sheet. Each table should be
headed by a brief legend.

Figures and plates

Figures must be carefully prepared and should be submitted ready for publication.
Each should have a short legend, listed on a sheet following the literature cited.

Text figures should be in black ink and completely lettered. Keep in mind page format
and column size when designing figures.

Photographs for half-tone plates must be of good quality. They should be trimmed off
squarely, arranged into plates, and mounted on suitable drawing board. Where necessary,
a scale should be put on the actual figure. Preferably, photographs should be in the
desired final size.

It is the author’s responsibility that lettering is legible after final reduction (if any)
and that lettering size is appropriate to the figure. Charges will be made for necessary
alterations.

Processing of manuscripts

Upon receipt each manuscript is critically evaluated by at least two referees. Based on
these evaluations the editor decides on acceptance or rejection. Acceptable manuscripts
are returned to the author for consideration of comments and criticisms, and a finalized
manuscript is sent to press. The author will receive from the printer two sets of proofs,
which should be corrected carefully for printing errors. At this stage, stylistic changes
are no longer appropriate, and changes other than the correction of printing errors will
be charged to the author at cost. One set of corrected proofs should be returned to the
editor.

An order form for the purchase of reprints will accompany proofs. If reprints are
desired, they are to be ordered directly from the printer.

Send manuscripts, proofs, and correspondence regarding editorial matters to: Dr. David W.

Phillips, Editor, 2410 Oakenshield Road, Davis, CA 95616 USA.

CONTENTS — Continued

A new and polytypic species of Helminthoglypta (Gastropoda: Pulmonata) from
the Transverse Ranges, California.
BARRY JROTH yy ()2°) 2): S27. SRN aeolian ee epg ae Re eR ee 184

A new species of Naquetia (Muricidae) from the Gulf of Aqaba.
ANDEHONY, DZAGmIEIOVAND CAR OTE) ME MEI RSI:7/0 ee aye nena 190

Pyropeltidae, a new family of cocculiniform limpets from hydrothermal vents.
JAMES H. MCLEAN AND GERHARD HASZPRUNAR ..............----.-- 196

NOTES, INFORMATION & NEWS

Fact or Artifact?
So AAIN DERE RO Eid 505s cat uae oe ee een ae DL ge A 206

Response to “Fact or Artifact?” by S. van der Spoel.
RONALD, Wh. GIUMER a5 oN Seats Padi siege Stine St apreitr icy Ue thane 207

BOOKS PERIODICALS sa AMP EIEE Si aratgus nie ins an ene Mil

ISSN 0042-3211

V4
4

PTHE

& ELIGER

A Quarterly published by

CALIFORNIA MALACOZOOLOGICAL SOCIETY, INC. eer

Berkeley, California Mo ODD E py pas eee ‘a

R. Stohler, Founding Editor " -
FEB 05 1988

|

Volume 30 January“4, 1 188; ar mice fo Number 3

-CONTENTS

| The functional morphology of scaphopod captacula.
FAOUNV AUG Dg SEMIN ATE Gia ay Ve pea ree is yer. So per tals US cdl ys MEL LS 213

Ontogenetic change in the radula of the gastropod Epztonium billeeana (Proso-
branchia: Epitoniidae).
ANDREW OE L/AGESAND RICHARDG. WILLAN »22 2). o)2c. oJ eee bes es dae - 222

Illustrated embryonic stages of the eastern Atlantic squid Loligo forbes.
S. SEGAWA, W. T. YANG, H.-J. MARTHY, AND R. T. HANLON .......... 230

The red foot of a lepidopleurid chiton: evidence for tissue hemoglobins.
DouGLAS J. EERNISSE, NORA B. TERWILLIGER, AND ROBERT C. TERWILLI-
(GE Rea nr ee age gra a terse te MAD RAL lei by Ail ihe ce Mitts coh 3 Cele 3 a CaN Atte 244

Chromosomes of some subantarctic brooding bivalve species.
CATHERINE THIRIOT-QUIEVREUX, JACQUES SOYER, MARc Bouvy, AND JOHN
Jes, ANTLTETIINE hN2 Ca a0 ms cael aN Nd ne RS a eo a ee Ee 248

Reproduction and growth of the brooding bivalve Transennella tantilla.
WIARIVg MINING ASSON SD AUURIBS mime Eas cat ak ukds . veldgn aiiahaieyaedimneeis) eat. Lue cals 257

Aspects of the life history and population biology of Notospisula trigonella (Bi-
valvia: Mactridae) from the Hawkesbury Estuary, southeastern Australia.
em ONES W/Ate VW RAY WANE) Gera SKILLE DER 22 50 as tie bossa sees: 267

Reproduction in a brackish-water mytilid: gametogenesis and embryonic devel-
opment.
Re DERNARD bake DAVIES, “AND Ac Ni EIODGSON © 222.5--5 2.09021. 278

CONTENTS — Continued

The Veliger (ISSN 0042-3211) is published quarterly on the first day of July, October,
January and April. Rates for Volume 30 are $25.00 for affiliate members (includ-
ing domestic mailing charges) and $50.00 for libraries and nonmembers (including
domestic mailing charges). An additional $3.50 is required for all subscriptions sent
to foreign addresses, including Canada and Mexico. Further membership and sub-
scription information appears on the inside cover. The Veliger is published by the
California Malacozoological Society, Inc., % Department of Zoology, University of
California, Berkeley, CA 94720. Second Class postage paid at Berkeley, CA and
additional mailing offices. POSTMASTER: Send address changes to C.M.S., Inc.,
P.O. Box 9977, Berkeley, CA 94709.

THE VELIGER

Scope of the journal
The Veliger is open to original papers pertaining to any problem concerned with mol-
lusks.

This is meant to make facilities available for publication of original articles from a
wide field of endeavor. Papers dealing with anatomical, cytological, distributional, eco-
logical, histological, morphological, physiological, taxonomic, etc., aspects of marine,
freshwater, or terrestrial mollusks from any region will be considered. Short articles
containing descriptions of new species or lesser taxa will be given preferential treatment
in the speed of publication provided that arrangements have been made by the author
for depositing the holotype with a recognized public Museum. Museum numbers of the
type specimen must be included in the manuscript. Type localities must be defined as
accurately as possible, with geographical longitudes and latitudes added.

Very short papers, generally not exceeding 500 words, will be published in a column
entitled “NOTES, INFORMATION & NEWS’; in this column will also appear notices
of meetings, as well as news items that are deemed of interest to our subscribers in
general.

Editor-in-Chief
David W. Phillips, 2410 Oakenshield Road, Davis, CA 95616, USA

Editorial Board

Hans Bertsch, National University, Inglewood, California

James T. Carlton, University of Oregon

Eugene V. Coan, Research Associate, California Academy of Sciences, San Francisco
J. Wyatt Durham, University of California, Berkeley

Terrence M. Gosliner, California Academy of Sciences, San Francisco
Cadet Hand, University of California, Berkeley

Carole S. Hickman, University of California, Berkeley

David R. Lindberg, University of California, Berkeley

James H. McLean, Los Angeles County Museum of Natural History
Frank A. Pitelka, University of California, Berkeley

Peter U. Rodda, California Academy of Sciences, San Francisco

Clyde F. E. Roper, National Museum of Natural History, Washington
Barry Roth, Santa Barbara Museum of Natural History

Judith Terry Smith, Stanford University

Ralph I. Smith, University of California, Berkeley

Wayne P. Sousa, University of California, Berkeley

T. E. Thompson, University of Bristol, England

Membership and Subscription
Affiliate membership in the California Malacozoological Society is open to persons (no
institutional memberships) interested in any aspect of malacology. As an affiliate member,
a person may subscribe to The Veliger for US $25.00 (Volume 30), which now includes
mailing charges to domestic addresses. There is a one-time membership fee of US $2.00,
after payment of which, membership 1s maintained in good standing by the timely renewal
of the subscription; a reinstatement fee of US $3.00 will be required if membership
renewals do not reach the Society on or before April 1 preceding the start of the new
Volume. If a receipt is required, a self-addressed, stamped envelope (or in the case of
foreign members, the envelope and two International Postal Reply coupons) should be
included with the membership or subscription request.

The annual subscription rate to The Veliger for libraries and nonmembers is US $50.00
(Volume 30), which now includes mailing charges to domestic addresses.

An additional US $3.50 is required for all subscriptions sent to foreign addresses,
including Canada and Mexico.

Memberships and subscriptions are by Volume only (July 1 to April 1) and are payable
in advance to California Malacozoological Society, Inc. Single copies of an issue are US
$25.00 plus postage.

Send all business correspondence, including subscription orders, membership applications,
payments for them, changes of address, to: C.M.S., Inc., Post Office Box 9977, Berkeley,
CA 94709, USA.

Send manuscripts, proofs, books for review, and correspondence regarding editorial matters
to: Dr. David W. Phillips, Editor, 2410 Oakenshield Road, Davis, CA 95616, USA.

The Veliger 30(3):213-221 (January 4, 1988)

THE VELIGER
© CMS, Inc., 1988

The Functional Morphology of Scaphopod Captacula

by

RONALD L. SHIMEK'!

Bamfield Marine Station, Bamfield, British Columbia, Canada VOR 1B0

Abstract. Captacular functional morphology was examined in Dentalium rectius, Cadulus aberrans,
and Pulsellum salishorum by examination of histological sections, scanning electron microscopy, and
observation of living individuals. Subsidiary information was obtained from scanning electron microscopy
of C. tolmie: and D. pretiosum. The captacular morphology of all these species is similar except for the
ciliation and internal musculature of the captacular stalk. Dentalium species have a complete ciliated
band running the length of the captacular stalk. Cadulus species have a sequence of ciliated tufts, and
Pulsellum species have no stalk ciliation. Dentalium has 8-10 longitudinal captacular retractor muscles
in the stalk, while the other genera have only six.

A captaculum is extended by the bulb cilia, which pull the captaculum out of the mantle cavity and
through the sediment. The captacula likely adhere to prey by the action of a dual-gland adhesive system.
At least two glandular secretions are released into the area of the pit that adheres to the prey. Contraction

of the stalk longitudinal muscles pulls the captaculum within the mantle cavity.
Dentalium uses the complete stalk ciliation to collect small particulate matter in a manner analogous
to terebellid polychaete tentacles. Cadulus can also do this, but only in some circumstances, while Pulsellum

cannot feed in this manner.

These differences in captacular stalk ciliation are reflected in the variety of prey consumed, and lead
directly to differential prey utilization and indirectly to differential habitat utilization by these species.

INTRODUCTION

Although widespread, scaphopods are poorly known. While
common in deep water, shallow water representatives are
seldom abundant enough for reliable collection and ob-
servation (MoRTON, 1959; JONES, 1964; CoAN, 1964;
Davis, 1968; GAINEY, 1972; MCFADIEN, 1973; BILYARD,
1974; Rokop, 1977; SCARABINO, 1979; CARTER, 1983). At
least six species in three nominal genera are found in the
shallow waters of Barkley Sound on the southwest side of
Vancouver Island, British Columbia, and three species are
common enough to be collected consistently, sometimes in
great abundance.

Scaphopods have been called “the most homogeneous
class of mollusks” (MoRTON, 1959). Within any sympatric
assemblage of closely related organisms, behavioral or
structural modifications resulting in differential resource
utilization are likely to have arisen. In the course of an
investigation of the ecological interactions of this particular
scaphopod assemblage (Shimek, in preparation), I ex-
amined the functional morphology of scaphopod prey cap-

' Present mailing address: P.O. Box 69793, Seattle, Washing-
ton 98168, U.S.A.

ture, manipulation, and feeding. Dietary resources are
commonly partitioned in marine mollusks, particularly
among benthic predators (KOHN, 1959; KOHN &
NYBAKKEN, 1975; SHIMEK, 1983a, b). Thus, differences in
the means of prey capture and feeding are important, and
fundamental, to the success and diversity of these groups.
Captacula, characteristic of scaphopods, are small, elon-
gate, retractile tentacles originating lateral to the base of
the buccal pouch or proboscis. Typically several hundred
tentacles are found, but in smaller individuals, less than a
hundred may be present (MorTON, 1959) (Figure 1). Al-
though they clearly function in prey capture and manip-
ulation, the full range of captacular action in a normal
situation has never been clearly documented (MORTON,
1959; DINAMANI, 1964; GAINEY, 1972; BILYARD, 1974;
Poon, 1987). This is due to the infaunal habitat of the
animals, and the fact that, if disturbed, they may take
several hours or days to resume normal behavior.
Captacula have been observed adherent to potential prey
items (MORTON, 1959; GAINEY, 1972; BILYARD, 1974) and
it has been presumed that they function to pull larger prey
into the mantle cavity. DINAMANI (1964) and GAINEY (1972)
have observed particulate transfer up the captacular stalk
in Dentalium, and POON (1987) documented a similar

Page 214 The Veliger, Vol. 30, No. 3

R. L. Shimek, 1988

Page 215

Table 1

Scaphopod collection sites, with depth, substrate type, and species collected.

Mayne Bay Imperial Eagle Channel Trevor Channel Sarita Bay
Sites (48°58.7'N, 125°19.5'W) — (48°52.7'N, 125°11.4'W) = (48°49.7'N, 125°11.0'W) = (48°53.5'N, 125°03.0'W)
Depth 35-40 m 75-80 m 30-110 m 120-200 m
Substrate type silt silt sand silt

Species collected Dentalium rectius

Pulsellum salishorum

* Rare at this site.

process in Cadulus tolmie:. Although the anatomy of Den-
talium captacula has been described (MORTON, 1959;
FISHER-PIETTE & FRANC, 1968), the mechanism for either
adherence to large particles or small particulate transfer
has not been thoroughly investigated.

In the present study, I examined fixed captacula from
individuals of Dentalium rectius Carpenter, 1864; D. pre-
tiosum Sowerby, 1860; Cadulus aberrans Whiteaves, 1887;
C. tolmie: Dall, 1897; C. californicus Pilsbry & Sharp, 1898;
and Pulsellum salishorum Marshall, 1980. Furthermore, I
examined captacular action in living specimens of C. aber-
rans, D. rectus, and P. salishorum with the objective of
determining the mode of captacular function, and the vari-
ation in function and morphology between these species.

MATERIALS anp METHODS

Specimens were dredged from Barkley Sound (Table 1)
and maintained in cooled seawater (=5°C) until they were
brought to the laboratory. Individuals to be examined alive
were rinsed clean of sediment from the shell apertures and
placed in a container of fresh sediment from their habitat.
Failure to clean the apertures of sediment generally re-
sulted in death, as the animals seemed incapable of re-
moving the impacted sediment. Specimen containers had
been modified with screens in the bottom to allow water
circulation through the sediment; thus no anaerobic sed-
iment developed. The containers were placed in sea tables

Dentalium rectius

Pulsellum salishorum
Cadulus aberrans*
Cadulus tolmiei*

Dentalhum rectius Dentalium rectius*
Dentalium pretiosum*
Pulsellum salishorum
Cadulus aberrans

Cadulus tolmiei*

Pulsellum salishorum

Cadulus tolmier

in a flow-through seawater system. The ambient seawater
temperature never exceeded 15°C.

Animals treated in this manner remained healthy, and
could be maintained in the laboratory longer than three
months. Allowing the animals to get warmer than 15°C,
failure to clean the sediment out of the shell, or placing
the animals in bowls with no water circulation resulted in
high mortality or aberrant behavior.

Live animals were observed in a refrigerated room, at
10°C, using a Wild M-5 Stereo Microscope. These animals
were placed in thin layers of sediment from their natural
habitat or in transparent sediments. If the sediment depth
was insufficient to allow the animals to maintain their
normal “‘concave-side up” orientation, they were braced
in that position by gluing them to glass microscope slides
with a drop of cyanoacrylic glue. There was no mortality
associated with this procedure and the animals could be
subsequently detached from the slide. Animals observed
at higher temperatures shed captacula, refused to feed or
burrow, and became moribund.

Transparent sediment was made using two methods.
The first used sieved crystalline cryolite (Na,AIF,). Al-
though this method initially appeared to be satisfactory,
subsequent observations indicated cryolite was toxic, and
caused captacular shedding, prolonged retraction, and death.
Captacula were seldom shed when observed in a substrate
of transparent seawater agar.

Transparent agar, made by boiling a 1% (by weight)

Figure 1

Scale bar = 100 um in 1A, 10 um in all others. A. Pulsellum salishorum. Dorsal view, shell and mantle removed.
F, foot; L, proboscis lips. Arrow indicates an immature captaculum. B. Pulsellum salishorum. Single captaculum.
Note ciliated bulb and, except for a small distal fringe, the lack of ciliation on the captacular stalk. C. Cadulus
tolmier. Single captaculum. Arrow indicates gap in ciliated band. Note the ciliated bulb and that the ciliated tract
is completed distally. Compare with Figure 1F. D. Cadulus aberrans. Single captaculum. Note how the ciliated
band on the stalk becomes incomplete and tufted proximally. E. Cadulus aberrans. Proximal captacular stalk. Note
that the ciliary tufts are distinct. F. Cadulus tolmie:. Captacular stalks. Foreground stalk is distal and contracted;
note how the ciliated tufts act to form a band. Arrow indicates an isolated ciliary tuft on an elongated captacular
stalk. G. Dentalium rectius. Captacula. Note the complete band of cilia on the stalks. Metachronal ciliary beating
is evident on the captacular bulbs. H. Dentalium pretiosum. Captaculum. Note the complete ciliary bands visible in

the foreground and in the background.

Page 216 The Veliger, Vol. 30, No. 3

” f]
in,
|

'
a

: ef ae »
Ss 4/

R. L. Shimek, 1988

suspension of agar in seawater for 1 h with distilled water
added periodically to maintain the water level, was cooled,
forced through a 250-um screen, and allowed to settle to
a depth of 1-3 cm in transparent containers. After these
containers were carefully submerged in a sea table and a
bacterial growth had developed, Dentalium rectius could
be maintained in them for at least two months. If live
foraminiferans were added to the vessels subsequent to the
bacterial film development, Cadulus aberrans or Pulsellum
salishorum could also be maintained, although for shorter
periods.

Scaphopod behavior and captacular action could be ob-
served in these containers if they were handled gently.
When the animal was close to the substrate surface, cap-
tacular and foot movements in prey manipulation and
capture were clearly visible.

Animals to be sectioned were brought to the laboratory,
cleaned of sediment, placed in bowls of fresh seawater,
and maintained at <10°C overnight. They were fixed and
concurrently decalcified in Bouin’s fluid made with sea-
water, dehydrated, imbedded in synthetic paraffin, and
sectioned at either 8 or 15 wm. Various sections were
stained either with a modification of Masson’s triple stain
(SHIMEK, 1975), or with hematoxylin and eosin.

For scanning electron microscopy, the animals were fixed
for 1 h in phosphate-buffered 2.5% glutaraldehyde and
post-fixed for 1 h in 2% osmium tetroxide buffered in
sodium bicarbonate. The specimens were rinsed, dehy-
drated, and stored in 100% ethanol. The specimens were
critical point dried, mounted on stubs, gold coated, and
observed on a JEOL JSM-35 scanning electron micro-
scope.

Voucher specimens of the following species have been
deposited as the indicated lots in the Los Angeles County
Museum of Natural History: Dentalium rectius no. 124485;
Pulsellum salishorum no. 124486; and Cadulus aberrans no.
124487. Voucher specimens of C. tolmize: have been de-
posited in the mollusk collection of the U.S. National Mu-
seum of Natural History as lot no. 859073.

Buccal contents were obtained by dissection of the buccal
pouches (proboscides) of animals fixed immediately upon
collection, and stained with Rose Bengal, which allowed

Page 217

the determination of which prey had been alive when fixed
(BILYARD, 1974). The buccal pouch contents were ex-
amined, and live organisms, or organism remains, were
identified to the lowest possible systematic category. All
other ingested items were identified as precisely as possible.

RESULTS

External Captacular Morphology

The basic captacular anatomy was similar in all the
scaphopods examined. Although there were some differ-
ences in the relative dimensions of the captacula examined,
they were small, and were likely due to the relative sizes
of the animals examined, with larger animals having larger
captacula. The captacula arose as slender stalks from a
proliferative region on either side of the buccal pouch. Each
mature captaculum terminated in a ciliated bulb, contain-
ing a pit, the alveolus of MORTON (1959), on one surface
(Figure 1). The alveolus enlarges as the captaculum grows
and lengthens. The terminal bulb was ovoid and ciliated
on all surfaces, including the pit. These cilia, which beat
metachronally and continuously (Figure 1G), extended the
captacula out of the mantle cavity and through the sub-
strate.

As the captacula extended, the captacular stalk muscles
were relaxed and the stalk was stretched passively. In large
(aperture width = 2.0 mm) Dentalium rectius, the captac-
ula often extended 6 mm, and occasionally I was able to
measure them extended as far as 10 mm from the aperture.

The captacular stalk ciliation varied between the genera
examined (Figure 1). The Dentalium species had a narrow,
but complete ciliated tract running from the terminal bulb
down the stalk to the base. Species of Cadulus lacked the
complete tract, but had regularly spaced ciliated tufts, while
Pulsellum salishorum lacked any stalk ciliation (Figure 1).

Internal Captacular Morphology

The captacular stalk was covered with a thin squamous
epithelium. Below a narrow basement membrane were
longitudinal muscles that shorten the stalk, retracting the
captaculum. In Dentalium there were usually eight or more

Figure 2

Scale bar = 10 wm. All sections are 8 um in thickness, and all have been photographed using Nomarski differential
interference microscopy. A. Dentalium rectius. Captacular stalks. Arrow indicates a glancing longitudinal section;
note helically arranged muscles in the captacular stalk. In the transverse sections of captacular stalk, note the thin
squamous epithelium (the ciliary band is visible on most sections) and the 8-10 captacular stalk retractor muscles
just below the epithelium. B. Cadulus aberrans. Captacular stalks. Transverse sections. Note only 6 longitudinal
captacular stalk retractor muscles. C. Pulsellum salishorum. Captacular stalks. Transverse sections. Note only 6
longitudinal captacular stalk retractor muscles. D. Dentalium rectius. Captacular bulb. Near mid-sagittal section.
Arrow indicates opening of basal glands. E. Dentalium rectius. Captacular bulb. Oblique frontal section. G, basal
glands. Arrows indicate duct of basal glands. F. Dentalium rectius. Captacular bulb. Distal transverse section. Arrows
indicate pit glandular areas not associated with the basal glands. G. Dentalium rectus. Captacular bulb. Lateral
sagittal section in area of ciliary pit. Arrows indicate pit glands not associated with the basal glands.

Page 218

muscle cells; in Cadulus and Pulsellum there were six (Fig-
ures 2A-C). Occasionally small cellular processes were
seen in the stalk; these were likely nerves.

The captacular bulb contained at least two types of
secretory cells. Typically two large globular cells, found
near the proximal end of the bulb, contained a diffuse
granular secretion. Careful examination of serial sections
showed these cells emptied their products into the captac-
ular pit through long ducts that terminated in the distal
lateral margins of the pit (Figures 2D, E). Smaller, narrow
cells adjacent to the pit also contained similar, although
more intensely staining, secretory products. These cells
also discharged into the pit lumen through ducts termi-
nating in the bottom or sides of the pit (Figures 2F, G).

The longitudinal muscles of the captacular stalk were
lacking in the bulb; however, oblique muscles were found
just below the ciliated squamous epithelium. The mus-
culature around the ciliated pit was diffuse; although mus-
cle fibers did attach to the basement membrane in that
region, they were few and slender (Figures 2D-F). Several
other cell types were found in the bulb, and a faintly
staining region corresponding to the ganglion described by
Plate (1892, in FISHER-PIETTE & FRANG, 1968) was pres-
ent (Figure 2D).

Observed Captacular Function

The basic captacular functions were similar in the three
genera. Active muscular contraction did not cause exten-
sion of the captacula. The captacula were extended by the
action of cilia on the bulb, and retracted by muscular
contraction in the stalk. When the bulb was about to adhere
to some item, the bulb moved over it until the pit was
positioned on the surface. The bulb flattened slightly bring-
ing the pit into contact with the surface of the item. In
most cases the pit was moved from place to place over the
item until the captaculum stopped moving and abruptly
fastened to it. Shortly thereafter the captaculum stalk con-
tracted and the bulb was obviously adherent. There was
no appreciable deformation of the bulb when adhesion
occurred. Similarly, there was no noticeable change in
shape if the bulb detached from the item.

The connection between the bulb and the object was
strong; the active contraction of less than five captacula
pulled a foraminiferan that was 100 um in diameter free
of the sediment, through the feeding cavity, and into the
mantle cavity.

Captacula were often sloughed, particularly in stressed
animals. Autotomized captacula were never seen to become
adherent. Conversely, if they were autotomized after ad-
hering to an object, they were not seen to release. Captacula
appear to be regenerated easily, and in many sections and
some scanning electron micrographs, immature captacula
are recognizable (Figure 1A).

Captacula also manipulated food inside the mantle cav-
ity. Small specimens of Dentalium rectius, Cadulus aberrans,
and Pulsellum salishorum have transparent shells and man-

The Veliger, Vol. 30, No. 3

tles, and captacular action was easily observed within the
mantle cavity. Food items were brought into the mantle
cavity by contraction of adherent captacula, or by the action
of the foot. In the latter cases, the foot would scoop the
food item and some sediment into the mantle cavity using
the dorsal depression (Dentalium), or sediment would ad-
here to the side of the foot (Cadulus or Pulsellum). In any
event, no food item was taken directly to the mouth. Instead
the item was manipulated and moved vigorously around
within the mantle cavity. Most items brought into the
mantle cavity were subsequently released by all captacula,
and settled to the floor of the mantle cavity. These items
were regularly ejected from the mantle cavity by a con-
traction of the foot, which expelled fluid and particulate
matter from the mantle cavity.

Acceptable items were brought, by captacula, to the
densely ciliated lips (Figure 1A) which engulfed them.
Food was held within the buccal pouch for some time prior
to being masticated by the radula. Although the amount
of time food was held varied with the species and the
animal’s condition, most food items were ground up within
30 h (Shimek, in preparation).

Very fine sediment particles were also eaten (Table 2).
Dentalium rectius commonly collected sediment by moving
fine particles up the ciliated captacular stalk. Sediment
composed a substantially smaller dietary component of the
other genera (Table 2). Once sediment was moved into
the mantle cavity, it was collected and manipulated by the
captacular bulbs in a manner similar to the manipulation
of larger particulate material. Eventually a sediment bolus
was formed, passed to the mouth, and ingested.

Sediment was also collected by adhesion to the captacu-
lar bulb ciliated pit in Pulsellum and Cadulus, although I
never saw this mode of collection used by Dentalium. When
sediment was collected this way, it was drawn within the
mantle cavity by captacular contraction.

Captacula moved freely through all parts of the mantle
cavity, and were even seen extending from the dorsal ap-
erture. They appeared to collect mucus and perhaps ad-
herent particulate material from the ciliated ridges on the
lateral mantle wall. The fate of this collected material was
unclear.

DISCUSSION

The captacula are the major food-collection organs of
scaphopods. Although particulate food may sometimes be
brought into the mantle cavity by direct action of the foot,
particularly in the dentalioids, this is a relatively rare event
(Shimek, in preparation).

MortTon’s (1959) hypothesis of hydrostatic extension
of the captacula is clearly incorrect. The extension is en-
tirely due to the ciliated bulb, which moves in a manner
not unlike that of a ciliated protozoan. Captacula are slen-
der and their haemocoelic cavities are narrow; thus, the
fluid resistance within the stalk would be correspondingly
high. It is quite unlikely that muscular contractions around

Page 219

R. L. Shimek, 1988

89¢ c8 IIT 00SC C81 bol 89€ SOTO ORO ULLUN]
1810 brc0- SCO 6€1 0 c80°0 1800 94700 s}USWISeIy 182],
$90.0 1900 cLO'0 L800 990°0 680°0 S60°0 (ATuo sysa1) pea
90 19S°0 S6S 0 19Z°0 6cb 0 06c'0 Foc 0 NTL
SUBIIJIUTUILIOF
€L00 vel O SEO L100 bcr'0 Ors 0 S90 MMA EOC |AROIL,
c10'0 S00°0 1S0'0 brl oO 6L0°0 PHYO
L200 0s0'0 L60°0 0z10 s332 podomiy
Lc0'0 Lc0'0 180°0 9L0°0 sjaqjed yeoaq
S900 S80°0 Lc0'0 c10°0 £600 €L00 Lc0'0 suIeIs [PIQUIT
800°0 L¢0'0 ¥S0'0 100°0> 0c 0 SPL O £90 SLY OE] MAUI NS
uonsodosd sjuajuo0s [eoong
oLL0 ce9 0 18S°0 6860 6LS°0 169°0 Ss90 Sutpeey uonsodo1g
€S ve SC 98 br LY SS SEEMED)
yeoonq YIM Joquinny
89 BE cy 48 OL 89 v8 Pour XS
Jaquinu [e107
Jouueys) J10Ad1 7, ‘UD 9[8eq [euoduy Aeg aude] JauueYy) JOA y «=. [aUULYD JOA], “YD aseq jeusdwy Aeg audeyy ‘IMS UONI2T[OD
wWNLOYSYDS UNIJaS|Ng wUNLOYSIDS WN]Jasjng wWiNLOYSIIDS WN]JasjNq ——- SuUDLLaQD SRINPDD = SN1JIaL WNYDJUaG «= SN4yjda4 WNYDJUagq =—- SN4J9a4 NID] Ua :satvadg

‘sdus da1y41 1e spodoydesds jo satoads aar1y1 UO UONeUTIOJUT }U9}U09 [eoonNg Jo ArewUINS

G IRMA

Page 220

any portion of the haemocoel could result in appreciable
or even noticeable extension of a captaculum.

Captacular bulb adhesion in scaphopods was proposed
to occur as a muscular suction cup (MorRTON, 1959). Active
muscular suction is unlikely for several reasons. First,
when adhesion of a bulb to a prey item occurs, and then
that captaculum is shed, the bulb remains adherent to the
item. Secondly, during adhesion no bulb deformation oc-
curs. The muscular contraction necessary for active suction
adhesion would certainly deform the bulb’s opposite side
as well as the pit, and would relax, causing detachment
upon shedding of the captaculum. Thirdly, the bulb, in-
cluding the pit, is covered with a dense ciliary layer. An
active ciliary covering would seem to preclude the necessary
seal for suction to occur unless substantial mucous secre-
tions are involved. There are no indications of any such
secretions (Figure 1). Finally, sections of the bulb indicate
relatively few muscles. It seems unlikely these few muscles
could maintain the suction necessary to pull the relatively
bulky prey through sediment.

A more plausible hypothesis involves the action of a
dual-gland adhesive system (HERMANS, 1983). The large
glands at the base of the bulbs with their relatively diffuse
secretions, and the small glands with dense secretory gran-
ules near the pit, both empty into the bulb pit or its edges.
These two glands correspond well, in gross structure, to
descriptions of the dual-gland adhesive systems now seen
in several invertebrate taxa (HERMANS, 1983). If these
secretions were under neural control, it would explain why
shed captacula do not detach from adherent items or tightly
adhere to any item. Furthermore, the lack of captacular
deformation is explained by this hypothesis. Finally, while
some muscularity of the bulb is necessary to allow defor-
mation and ease of movement through sediment interstices,
the large active muscles needed to form an active suction
cup are lacking. The lack of such a muscular component
is easily explained by the hypothesis of a dual-gland ad-
hesive system.

The pit in the captacular bulb is the place of adhesion,
and is likely the major sensory area of the captacular bulb
as well. It appears as if, prior to adhesion, the pit area is
the site of prey item assessment.

In my histological sections a pale, faintly staining region
corresponding in location to the described nerve ganglion
can be demonstrated, and these cells may be neural in
origin. Ultrastructural examination should confirm the
presence of such a ganglion, and the associated sensory
neurons.

Although the muscular component of the captacular
bulb is weak and diffuse, that of the captacular stalk is
large and evident. Either 6, in Cadulus or Pulsellum, or 8-
10, in Dentalium rectius, longitudinal smooth muscle cells
were found surrounding the captacular stalk lumen. Den-
taluum entalis is described as having 10 longitudinal muscles
(MorTon, 1959). The cells are staggered along the length
of the stalk, and are helically arranged (Figure 1A). Mus-
cular contraction results in the shortening of the extended
stalk and rapid retraction of the unattached captacula. The

The Veliger, Vol. 30, No. 3

presence of six longitudinal muscles in the representatives
of the Siphodentalioidea and more than six in the Den-
talioidea may be of use as a systematic character; however,
more representatives in both orders should be examined.
The functional significance of such a difference is unclear.

Sediment has been seen moving on the captacular stalk
in both Dentalium and Cadulus (DINAMANI, 1964; GAINEY,
1972; Poon, 1987; Shimek, present study); however, the
mechanism for this movement was not previously clearly
described. In D. rectius the ciliated captacular stalk allows
a substantial amount of sediment to be collected. A similar
ciliated tract has been reported for D. entalis by Fol (1889,
in MorTon, 1959), although Morton could not demon-
strate it. In light of the presence of such a band on the
captacula of the two Dentalium species examined here, the
lack of noticeable ciliation in Morton’s sections is likely
due to a fixation artifact. This feeding mode is common
in D. rectius from Barkley Sound. Sediment is a major
dietary component, particularly in small animals (total
length < 10 mm), where more than 75% of the hindgut
contents is sediment. Dentalium rectius seldom grinds fo-
raminiferan or other particulate prey beyond recognition,
and consequently the amount of sediment ingested can
easily be assessed. Most, if not all, of this sediment is
collected by the captacular stalk ciliation.

Although the captacular stalk ciliation has been seen to
move particles into the mantle cavity in one Cadulus species
(Poon, 1987), it is unclear under what conditions this is
an important process. The tufted stalk ciliation found in
Cadulus may be unable to move much sediment if the stalk
is maximally extended. POON (1987) examined C. tolmiez,
which lives in silty habitats. My data indicate that while
C. aberrans, which lives in relatively clean sand, does oc-
casionally eat sediment, it is much more realistically termed
a foraminiferan dietary specialist. Perhaps the tufted stalk
ciliation pattern is important for sediment collection only
in those species common in fine sediment.

Pulsellum salishorum is unable to move any particulate
matter in this manner, as it lacks stalk ciliation altogether.
This species specializes upon foraminiferans, although
sediment is also occasionally found in the diet. This sed-
iment is likely collected only in the captacular pit or by
the foot.

The differences in the captacular structure are reflected
in the diets of the species examined, and serve to explain
some of the dietary differences. Dentalium rectius can collect
sediment regardless of its habitat owing to the possession
of a complete ciliated tract on the stalk of the captacula.
Cadulus species appear to be able to transport some sedi-
ment into the mantle cavity using their tufted stalk cilia-
tion, but this feeding mode is important only in C. tolmzez,
which lives in sediment dominated by silt-clay; C. aberrans,
found in sand, eats virtually no sediment. Finally, Pulsel-
lum salishorum, which has no ciliation on the captacular
stalk, ingests small quantities of sediment in all habitats.
This sediment is brought into the mantle cavity either by
adhesion to the bulb pit or the foot.

Thus, the specialization of Cadulus aberrans upon fo-

R. L. Shimek, 1988

Page 221

raminiferan prey is due, at least in part, to captacular
structure. In the habitat where this species is common,
foraminiferan prey can be collected by the captacula. Min-
eral grains in this habitat are too large to be transported
by tufted ciliation, and fine sediment particles may be too
infrequent to be effectively collected by pit adhesion. Pul-
sellum salishorum, from the same habitat as C. aberrans,
collects substantially less fine sediment to be formed into
boluses than it does in either of its other habitats (Table
2). All sediment collected by this species must be collected
by bulb adhesion or by the foot. Fine sediment may be too
uncommon in the well-sorted sand of the Trevor Channel
site to be efficiently collected by any but the completely
ciliated tract of Dentalium rectius. Thus, although all
scaphopods appear to be able to utilize their captacula for
the collection of relatively large particulate prey such as
foraminiferans, small bivalves, or kinorhynchs, only one
genus has the ability to efficiently collect large amounts of
small, silt-clay sized, sediment particles. This ability ap-
pears to give D. rectius a functionally defined competitive
advantage over the foraminiferan predators such as C.
aberrans in habitats with a large silt-clay fraction and small
numbers of foraminiferans, and undoubtedly contributes
to the widespread distribution of this common species.

ACKNOWLEDGMENTS

This study was supported in large part by the Bamfield
Marine Station. Additional financial support came from
the Pacific Northwest Shell Club, and the University of
Washington Friday Harbor Laboratories. The scanning
electron microscopy was done at the Biology Department,
University of Victoria, Victoria, B.C. I thank the Directors
of the Bamfield Marine Station and the University of
Washington Friday Harbor Laboratories for the permis-
sion to use those facilities. Dr. D. A. Thomson of the
University of Arizona generously allowed the use of his
laboratory during a portion of this study. I thank the
following individuals for assistance: A. Bergey, J. Dietrich,
J. Elliott, R. Fredrickson, J. Glazier, S. Leader, S. Rum-
rill, C. Singla, S. Tveit, and R. Warren.

LITERATURE CITED

BiLyarD, G. R. 1974. The feeding habits and ecology of Den-
talium entale stimpsoni Henderson (Mollusca: Scaphopoda).
Veliger 17:126-138.

CarTer, M. S. 1983. Interrelation of shell form, soft part
anatomy and ecology in the Siphonodentalioida (Mollusca,
Scaphopoda) of the northwest Atlantic continental shelf and
slope. Ph.D. Thesis, University of Delaware, Lewes, Del-
aware. xvi + 214 pp.

Coan, E. 1964. The Mollusca of the Santa Barbara County
area. Part I. Pelecypoda and Scaphopoda. Veliger 7:29-33.

Davis, J. D. 1968. A note on the behavior of the scaphopod,
Cadulus quadridentatus (Dall) 1881. Proc. Malacol. Soc. Lond.
38:135-138.

DinaMANI, P. 1964. Feeding in Dentaliwm conspicuum. Proc.
Malacol. Soc. Lond. 36:1-5.

FISHER-PIETTE, E. & A. FRANC. 1968. Classe des Scaphopodes.
In: P. P. Grasse (ed.), Traite de zoologie: anatomie, syste-
matique, biologie. Mollusques, Gasteropodes et Scapho-
podes. Tome 5:Fasc. III:987-1017.

Gainey, L. F., JR. 1972. The use of the foot and the captacula
in the feeding in Dentalium. Veliger 15:29-34.

HERMANS, C.O. 1983. The duo-gland adhesive system. Ocean-
ogr. Mar. Biol. Ann. Rev. 21:283-339.

Jones, G. F. 1964. The distribution and abundance of subtidal
benthic Mollusca on the mainland shelf of southern Cali-
fornia. Malacologia 2:43-68.

Koun, A. J. 1959. The ecology of Conus in Hawaii. Ecol.
Monogr. 29:47-90.

Konn, A. J. & J. W. NYBAKKEN. 1975. Ecology of Conus on
eastern Indian Ocean fringing reefs: diversity of species and
resource utilization. Mar. Biol. 29:211-234.

McFapien, M.S. 1973. Zoogeography and ecology of seven
species of Panamic-Pacific scaphopods. Veliger 15:340-347.

Morton, J. E. 1959. The habits and feeding organs of Den-
talium entalis. Jour. Mar. Biol. Assoc. U.K. 38:225-238.

Poon, P. 1987. The diet and feeding behavior of Cadulus tolmiei
Dall, 1897 (Scaphopoda, Siphonodentalioida). Nautilus 101:
88-92.

Roxop, F. J. 1977. Seasonal reproduction of the brachiopod
Frieleia halli and the scaphopod Cadulus californicus at bathy]
depths in the deep sea. Mar. Biol. 43:237-246.

SCARABINO, V. 1979. Les scaphopodes bathaux et abyssayx de
PAtlantique occidental (Systematique, distributions, adap-
tations). Nouvelle classification pour l’ensemble de la classe.
Doctoral Thesis, Universite d’Aix-Marseille II. U. E. R.
des Sciences de la Mer et de l’Enveronment. 154 pp.

SHIMEK, R. L. 1975. The morphology of the buccal apparatus
of Oenopota levidensis (Gastropoda, Turridae). Z. Morph.
Tiere. 80:59-96.

SHIMEK, R. L. 1983a. Biology of the northeastern Pacific Tur-
ridae. I. Ophiodermella. Malacologia 23:281-312.

SHIMEK, R. L. 1983b. The biology of the northeastern Pacific
Turridae. II. Oenopota. Jour. Moll. Stud. 49:146-163.

The Veliger 30(3):222-229 (January 4, 1988)

THE VELIGER
© CMS, Inc., 1988

Ontogenetic Change in the Radula of the Gastropod

Epitonium billeeana (Prosobranchia: Epitonidae)

ANDREW J. PAGE AND RICHARD C. WILLAN

Department of Zoology, University of Queensland, St. Lucia,
Brisbane, Queensland 4067, Australia

Abstract.

Epitonium billeeana (DuShane & Bratcher, 1965) is identified and described from the Great

Barrier Reef, Australia. Like other epitoniids, E. billeeana was found to be a protandric hermaphrodite,
changing sex between 8.6 and 12.7 mm shell length. Middle lateral radular teeth change within a
particular row with growth, from a relatively small denticulate structure to a larger smooth structure.
Transitional radulae are identified. We suggest the radula change is mediated or instigated by the
change from the male to the female reproductive state.

INTRODUCTION

One of us (A.J.P.) is currently investigating the ecology
of coral eating gastropods on Australia’s Great Barrier
Reef. A thin-shelled wentletrap is moderately abundant
on middle- and outer-shelf coral reefs where it is obligately
associated with scleractinian corals belonging to the family
Dendrophylliidae. Not only does this epitoniid feed exclu-
sively on two particular species of dendrophylliid coral,
but the animal also resembles these host corals by being
vivid golden-yellow in color; such pigmentation is an out-
standing exception for a family whose other members are
all generally white. This distinctive epitoniid has been
known from Australia as the “golden wentletrap” for a
decade and figured in color in several publications
(MacLEIsH, 1973; COLEMAN, 1978, 1981; ENDEAN, 1982;
RUDMAN, 1984) but no specific name has been attached
to it. We show here it is referable to an eastern Pacific
taxon, Epitonium billeeana (DuShane & Bratcher, 1965).
The species’ full range extends, in tropical waters,
throughout the Pacific and across the Indian Ocean to the
Maldive Islands.

In the course of studying the gut of Epitonium billeeana,
we made the unexpected discovery that an ontogenetic
change takes place in the shape of teeth within rows of its
radula. The purpose of this paper is to document this
significant change, which has not been hitherto suspected
in the Epitoniidae.

The ptenoglossan radula of epitoniids bears similar,
elongate teeth with or without denticles on the blade
(THIELE, 1928). As with most other gastropods possessing
a multiseriate radula, numbers of teeth and tooth size

increase with an individual’s growth (THOMPSON, 1958;
BERTSCH, 1976). Most species of epitoniids whose radulae
have been studied possess denticles (THIELE, 1928; CLENCH
& TURNER, 1952; Taki, 1956, 1957; DUSHANE &
BRATCHER, 1965; DUSHANE, 1974, 1979). None of these
authors reports any alteration in the presence of denticles
with growth in any species, so tooth shape has been as-
sumed to be invariable and hence specifically diagnostic,
as for most other gastropods (FRETTER & GRAHAM, 1962).
Here we report one clear instance where this is not the
case. We show that the teeth of Epitonium billeeana change
in shape within an individual as it grows.

MATERIALS anp METHODS

Epitonium billeeana was collected from its host corals, Den-
drophyllia gracilis Milne Edwards & Haime and Tubastrea
faulkneri Wells in 6 to 16 m on Heron and Wistari reefs
(23°27'S, 151°55’E) at the southern end of the Great Bar-
rier Reef in Queensland, Australia, in September 1984
and September 1985. Twenty-six specimens from 4.8 to
23.6 mm shell length were collected specifically to examine
their radulae. All were fixed in Bouin’s solution, which
decalcified the thin shells in three days. The gonad was
sectioned (6 um) to determine sex and sections were stained
using Mayer’s hematoxylin and 0.3% alcoholic eosin
(LuNA, 1968).

Two methods were used to prepare radulae for light
microscopy. In one, the pharyngeal mass was excised and
heated in 10% KOH at 100°C for 20 min. The isolated
radula was then rinsed in distilled water, blotted dry, stained
in acidic fuchsin (1 h), rinsed briefly (30 sec), and mounted

A. J. Page & R. C. Willan, 1988

Page 223

Figure 1

Epitonium billeeana, SEMs of shell. A. Whole shell (length = 4.9 mm). B. Protoconch (bar = 0.5 mm). C. Detail

of sculpture (bar = 100 um).

in polyvinyl-alcohol-lactophenol (PVA). The second meth-
od followed MIKKELSEN (1985). The excised pharyngeal
mass was placed in a marked well of a multi-well Boener
slide in 10% KOH at room temperature (20-27°C) for 24
h. The isolated radula was then stained briefly (approx-
imately 5 min) in acidic fuchsin before mounting in car-
boxymethyl-cellulose (CMC). For light microscopy, best
results were obtained following the techniques outlined by
MIKKELSEN (1985), except for larger radulae, which were
mounted in PVA which necessitated longer staining (1 h)
in acidic fuchsin. The more viscous PVA medium gave
greater control in manipulating radulae while they were
being mounted.

Radulae to be examined by the scanning electron mi-
croscope (SEM) were placed individually in small vials of
distilled water and ultrasonicated for 20 sec. Some were
attached to the flat surface of pin-type SEM stubs with
double-sided adhesive tape. In other preparations, copper
paint was dabbed onto the stub (to create an elevation on
the surface) and allowed to dry. Then glue from adhesive
tape, which had been obtained by brushing the tape with
a fine-tipped paint brush dipped in chloroform, was used
to attach the radulae to the paint spots. This latter tech-
nique produced better results in that relatively more rad-
ular teeth were available for examination.

All measurements of teeth were made with a calibrated

Page 224
A We oR
29
1 3 3
j Wa Yi, |

row 28

hil]

The Veliger, Vol. 30, No. 3
1A) |
4
45
yi, “

20pm

pm

2
© 24

25

st

4

Figure 2

Epitonium billeeana, radular teeth. A. Inner laterals (tooth numbers 1-3 counting outwards from the midline),
middle laterals (16, 17), outer laterals (29, 30), shell length = 6.4 mm. B. Inner laterals (1-3), middle laterals (23-
25), outer laterals (44-46), shell length = 23.6 mm. C. Middle lateral teeth from anterior (row 1) to posterior (row

28) tooth rows, shell length = 9.9 mm.

eye piece and drawings made with the use of a camera
lucida.

TAXONOMY

Epitonium billeeana (DuShane & Bratcher) is a distinctive
epitoniid because of its shell sculpture, animal pigmen-
tation, and habit of living obligately with dendrophylliid
corals. It was first described from the Gulf of California
(DUSHANE & BRATCHER, 1965) and is currently recog-
nized as being widespread in the Panamic Province of the
eastern Pacific Ocean (DUSHANE, 1967, 1974; KEEN, 1971).
Specimens from the eastern Pacific are identical with west-
ern Pacific and eastern Indian Ocean material, and we
have no hesitation in identifying them as E. billeeana.
ROBERTSON & SCHUTT (1984) provisionally applied this
name to Indo-Pacific populations of the “golden wentle-
trap.”

It is desirable to give a full synonymy so researchers
can consult literature on this species without being con-
fused by the different names that have been applied in
different countries.

Synonymy

Scalina (Ferminoscala) billeeana DUSHANE & BRATCHER, 1965:
160-161, pl. 24, figs. 1-4; DUSHANE & PoORMAN, 1967:
424.

Epitonium (Asperiscala) billeeana (DuShane & Bratcher):
DUSHANE, 1967:87; DUSHANE & MCLEAN, 1968:1, 2,
fig. 1.

Epitonium billeeana (DuShane & Bratcher): ROBERTSON,
1970:45.

Epitonium (Asperiscala) billeeanum [sic] (DuShane & Bratch-
er): KEEN, 1971:424, fig. 612; DUSHANE, 1974:9, 10,
figs. 13, 15, 155a, 155b; ROBERTSON & SCHUTT, 1984:
1, 4.

Epitonium sp.: MACLEISH, 1973:755 (photograph by V. Tay-
lor); COLEMAN, 1978:116; COLEMAN, 1981:13, 44;
ENDEAN, 1982:138, fig. 137; RUDMAN, 1984:172.

Epitonium sp. 5: LOcH, 1982:5, illust.

We share DUSHANE & BRATCHER’s (1965) and
ROBERTSON & SCHUTT’s (1984) uncertainty that Epitoni-
um is really the most appropriate genus-level taxon to
accommodate Scalina billeeana. The species does seem in-
congruous in that genus, but is more suitable there than
in Amaea or Cirsotrema. Proper generic allocation must
await a phylogenetic analysis of the entire family. The
specific name, billeeana, is a patronym honoring Ms. Billee
Dilworth. As such it is a non-Latin noun in apposition
and hence indeclinable, 1.e., its termination cannot be
changed to agree in gender with the generic name (“‘dil-
leeanum” is thus incorrect in the combination Epztonium
billeeanum, even though the gender of the Latin genus
Epitonium is neuter).

Description

The following brief description distinguishes Epitonium
billeeana from other, sympatric, Indo-Pacific congeners.

Shell (Figure 1A) to 25 mm in height. Protoconch (Fig-
ure 1B) high and conical, multispiral (3-4 whorled),

A. J. Page & R. C. Willan, 1988 Page 225

Figure 3

Epitonium billeeana, SEMs of radular teeth and coral spirocyst tubes. A. Denticulate middle lateral teeth, shell
length = 6.0 mm, bar = 10 um. B. Smooth middle lateral teeth, shell length = 21.3 mm, bar = 10 um. C. Teeth
with undischarged coral spirocyst tubes, shell length = 12 mm, bar = 10 um. D. Detail of spirocyst tube from C,
bar = 1 um.

possessing faint, opisthocline axial ridges, dull purple in median stripe; overlain by a thin, adherent, pale buff peri-
color. Teleoconch elongate, possessing 7 or 8, thin, globose, ostracum. Aperture circular, peristome vertical with a
strongly convex whorls when full grown; sutures deeply moderate anterior expansion. Shell umbilicate. Head-foot,
impressed; sculpture reticulate, consisting of equal, low, mantle and visceral mass of animal chrome-yellow; show-
rounded, spiral cords (12-15 on body whorl) that are over- ing everywhere through the shell in life.

ridden by numerous (60-130 on body whorl), sharp, axial

ridges (Figure 1C) each ridge elevated into a lamella where SEXUALITY

it crosses a spiral cord; sculpture weaker on body whorl

of adults, spiral cords predominating; color white, with a Like other wentletraps (ROBERTSON, 1981; Boss, 1982;

purplish hue extending to 4th teleoconch whorl as a thin MELONE, 1986), Epitonium billeeana is a protandric her-

Page 226

150

100

Longest middle lateral tooth (um)

50

0 10
Shell length (mm)

Figure 4

The Veliger, Vol. 30, No. 3

Y=1.74X + 101.8

Y = 2-28 X + 57-7

20

Epitonium billeeana, relationships between shell length and the length of the longest middle lateral tooth. (@)
Denticulate teeth, regression line Y = 2.28X + 57.7, r = 0.596, P < 0.1. (@) Smooth teeth, regression line Y =

1.74X + 101.8, r = 0.698, P < 0.05.

maphrodite. Based on our own observations on the state
of the gonad, males (with shell lengths from 4.8 to 12.3
mm) are generally smaller than females (8.6 to 23.6 mm).
Mature and developing spermatozeugmata and sperma-
tozoa (as figured by NISHIWAKI [1964], TocHIMOTO [1967],
and NISHIWAKI & TOCHIMOTO [1969]) were observed in
the testes of males and mature and developing ova were
present in the ovaries of females. When sampled, all fe-
males were identifiable by the presence of strings of egg
capsules.

RADULA DESCRIPTION

Epitoniids have a ptenoglossan radula, a broad structure
that possesses many lateral teeth but lacks a rachidian
(GRAHAM, 1965; Boss, 1982). Within the radula, each
row consists of two symmetrical halves. In that of Epztoni-
um billeeana, the inner laterals of every half row (z.e., those
teeth nearest the midline) are smallest. Moving outwards,
tooth size gradually increases to a maximum about halfway
along each half row. Beyond this point, tooth size gradually
decreases to the point where the outer laterals are only
slightly longer than the inner ones. Teeth of every half
row can thus be divided into three groups—inner, middle,
and outer laterals (Figures 2A, B). Similar changes in
relative tooth size across a half row have been noted in
some of the epitoniids examined by CLENCH & TURNER

(1952) and Taki (1956, 1957). Taki (1956) even segre-
gated the teeth of E. latifasciatum (Sowerby) into three
regions—inner, middle, and outer. All the teeth of E. bil-
leeana terminate with a single, pointed cusp and below the
cusp there may be up to seven prominent denticles along
the blade. The cusp is always larger than any of the den-
ticles. When a tooth possesses more than one denticle, that
immediately below the cusp exceeds all the others in length
(Figure 3A).

The radula of epitoniids covers the entire surface of the
odontophore, which is divided into halves by a deep, mid-
dorsal, longitudinal groove (GRAHAM, 1965). Conse-
quently radulae are extremely difficult to mount flat and
radular formulae are often difficult to determine precisely.
For this reason, it was only possible to count the numbers
of lateral teeth accurately in three radular preparations of
Epitonium billeeana. These, together with the length of
each specimen’s shell in parentheses, are as follows: 30 x
30.0.30 (6.4 mm); 39 x 40.0.40 (8.6 mm); 57 x 62.0.62
(15.9 mm).

ONTOGENETIC CHANGE

The large middle lateral teeth exhibit the greatest degree
of change with growth of an individual. The middle lateral
teeth of small Epitonium billeeana differ from those of large
E. billeeana in size and the presence or absence of denticles

A. J. Page & R. C. Willan, 1988

(Figure 4). Small specimens of E. billeeana (<8.6 mm)
were found to have comparatively small (average length
of longest middle lateral tooth 71 um), denticulate (3-7
denticles), middle lateral teeth (Figures 3A, C). Large E.
billeeana (>12.3 mm) were found to have longer (average
length of longest middle lateral tooth 133 um), smooth,
middle lateral teeth (Figure 3B). Wentletraps of inter-
mediate size (8.6-12.3 mm) were found to have middle
lateral teeth of intermediate size (average length of longest
middle lateral tooth 105 wm) which were either denticulate
(1-7 denticles) or smooth. Epitonium billeeana of inter-
mediate size with smooth middle lateral teeth also possess
at least some denticulate middle laterals at the anterior
end of their radula. In these cases (six examined) the oldest
middle lateral teeth are always denticulate and smaller
than the smooth, more recently formed middle lateral ones
nearer the germinal epithelium (Figure 2C). These rad-
ulae are in transition between possessing relatively small,
denticulate and longer, smooth middle lateral teeth. The
occurrence of transitional radulae in E. billeeana of inter-
mediate size demonstrates the change in tooth morphology
with ontogeny. Table 1 correlates the ontogenetic changes
of tooth morphology with sex in E. billeeana.

Through the courtesy of Mr. I. Loch of The Australian
Museum, Sydney, we were able to examine SEMs of rad-
ular teeth and the protoconch of a specimen from Christ-
mas Island, eastern Indian Ocean. These characters are
in agreement (in size and shape) with those described here
for Epitonium billeeana. Some of the teeth even have what
appear to be atrophied denticles indicating that they may
have come from a transitional radula. Unfortunately the
shell length of this Christmas Island specimen is not avail-
able.

The results presented here are at odds with DUSHANE
& BRATCHER’s (1965) description of the radular teeth of
Epitonium billeeana. Many of the radular teeth of their
7-mm specimen were figured as smooth or possessing only
a single denticle (DUSHANE & BRATCHER, 1965:pl. 24).
From our results (Figure 4), we would predict that all the
teeth of such a small individual should be denticulate. This
contradiction can perhaps be resolved by ontogenetic stud-
ies of the radulae of eastern Pacific material.

DISCUSSION

Reports of ontogenetic change in tooth morphology be-
tween rows in gastropod radulae are appearing more and
more frequently. Several authors have demonstrated that
the number of teeth within a half row increases as the
individual grows (e.g., STERKI, 1893; BERTSCH, 1976;
ROBERTSON, 1985). Beyond this simple allometric in-
crease, there are a few reports like this one of ours of
alteration in tooth morphology within a particular row
with growth. STERKI (1893) first described such changes
in the shape of teeth in some pulmonates, and CARRIKER
(1943) and HOLLISTER (1954) observed that the pattern
of denticulation of some prosobranchs’ teeth depended on
the size of the snail. MCLEAN & NYBAKKEN (1979) and

Page 227

Table 1

Epitonium billeeana. Changes in sex and radular tooth
morphology with growth of 26 specimens.

Num-
ber
Shell of
length speci-
(mm) Sex mens Radula description
<8.6 male 8 All teeth denticulate; 1-3 den-

ticles on inner laterals, 3—7
on middle laterals, 1-5 on
outer laterals.
8.6-12.3 male or 9 As above, or with smooth mid-
female dle lateral teeth posteriorly
and at least some denticulate
middle laterals anteriorly.
Middle lateral teeth smooth;
inner and outer laterals may
be denticulate (1 or 2 denti-
cles).

>12.3 female 9

NYBAKKEN (1970, 1981) reported that several species of
Conus changed their radula morphology with growth.
HICKMAN (1980) discovered ontogenetic change within rows
in the radula of Hipponix conicus (Schumacher). THOMPSON
& Brown (1984:11-17) described a ‘‘dental metamor-
phosis” in the opisthobranchs 77ritonia hombergi Cuvier
and 7. plebera Johnston wherein juveniles have denticulate
lateral teeth and adults have completely smooth laterals.
The rachidian teeth of several muricids alter with growth
(Fujioka, 1982, 1984a, b, 1985); for example, those of
Morula margariticola (Broderip) change from pentacuspi-
date to tricuspidate (FUJIOKA, 1984b). Most recently has
come the finding that denticulation of the “pseudocentral”’
tooth in the radula of T7icolia variabilis (Pease) also changes
with growth (ROBERTSON, 1985). All these reports indicate
that the phenomenon of ontogenetic change in tooth mor-
phology within particular rows may be more widespread
in the Gastropoda than previously suspected.

The most vexing question—what causes this altera-
tion—remains. Dietary change or sexual dimorphism seem
to be the two most probable explanations, yet neither ap-
pears, at the present time, to offer a satisfactory answer
for the observations. Our data on Epitonium billeeana pre-
sent some challenges to both these hypotheses. HICKMAN
(1980) and NYBAKKEN (1981) attributed changes in tooth
morphology to differing juvenile and adult diets. In the
case of EF. billeeana, small and large individuals occur, often
side by side, on exactly the same coral and they apparently
exhibit the same feeding behavior. Other evidence corre-
lates differing radular morphologies with the sex of an
individual; for example, the radula of male Drupella species
and 77icolia variabilis changes from a female-like state in
juveniles to the male state with sexual maturity (FUJIOKA,
1982; ROBERTSON, 1985 respectively). Our observations
on E. billeeana indicate the radular change may be sexually

Page 228

mediated, or at least instigated, but individuals apparently
switch sex from male to female before the radular change
is completed. The reason for the divergence of radular
tooth morphology between sexes, in both dioecious and
protandric hermaphrodite gastropods, may ultimately be
shown to be related to feeding efficiency and, hence, the
energy requirements of the sexually reproducing female
individual.

ACKNOWLEDGMENTS

The Director and staff of the Heron Island Research Sta-
tion are thanked for providing facilities for, and advice on,
research. The Hawaiian Malacological Society and the
Great Barrier Reef Marine Park Authority generously
provided financial support for field work (for A.J.P.). Mr.
I. Loch of The Australian Museum, Sydney, freely sup-
plied information on Christmas Island material. Ms. L.
J. Newman provided the scanning micrographs and Ms.
J. F. Rifkin identified coral spirocyst tubes. Drs. R. Rob-
ertson, T. S. Hailstone, and K. Warburton, Ms. L. J.
Newman, and Mr. R. H. M. Eertman are thanked for
reading the manuscript and offering criticisms. This study
was supported from funds from the Australian Universities
Grants Commission (to R.C.W.).

LITERATURE CITED

BERTSCH, H. 1976. Intraspecific and ontogenetic radular vari-
ation in opisthobranch systematics (Mollusca: Gastropoda).
Syst. Zool. 25:117-122.

Boss, K. J. 1982. Mollusca. Pp. 945-1116. In: S. P. Parker
(ed.), Synopsis and classification of living organisms. Vol. 1.
McGraw-Hill Book Co.: New York.

CARRIKER, M. R. 1943. Variability, developmental changes,
and denticle replacement in the radula of Lymnaea stagnalis
appressa Say. Nautilus 57:52-59.

CLENCH, W. J. & R. D. TURNER. 1952. The genera Epitonium
(part II), Depressiscala, Cylindriscala, Nystiella and Solutiscala
in the western Atlantic. Johnsonia 2:289-356.

COLEMAN, N. 1978. A look at the wildlife of the Great Barrier
Reef. Bay Books: Sydney. 128 pp.

COLEMAN, N. 1981. Shells alive. Rigby: Sydney. 94 pp.

DuSHANE, H. 1967. Epitonium (Asperiscala) billeeana (Du-
Shane & Bratcher, 1965) non Scalina billeeana DuShane &
Bratcher, 1965. Veliger 10:87-88.

DuSuHane, H. 1974. The Panamic-Galapagan Epitoniidae.
Veliger 16(Suppl.):1-84.

DuSHANE, H. 1979. The family Epitoniidae (Mollusca: Gas-
tropoda) in the northeastern Pacific. Veliger 22:91-134.
DuSHANE, H. & T. BRATCHER. 1965. A new Scalina from the

Gulf of California. Veliger 8:160-161.

DuSuaneE, H. & J. H. McLEAN. 1968. Three new epitoniid
gastropods from the Panamic province. Contrib. Sci. (Los
Angeles) 145:1-6.

DUSHANE, H. & R. POORMAN. 1967. A checklist of mollusks
for Guaymas, Sonora, Mexico. Veliger 9:413-440.

ENDEAN, R. 1982. Australia’s Great Barrier Reef. University
of Queensland Press: St. Lucia; London; New York. 348

PP-
FRETTER, V. & A. GRAHAM. 1962. British prosobranch mol-

Ihe Welicers Voles0 Noms

luscs: their functional anatomy and ecology. Ray Society:
London. 755 pp.

Fujioka, Y. 1982. On the secondary sexual characteristics found
in the dimorphic radula of Drupella (Gastropoda: Muricidae)
with reference to its taxonomic revision. Venus 40:203-223.

Fujioka, Y. 1984a. Remarks on two species of the genus Dru-
pella (Muricidae). Venus 43:44-54.

Fujioka, Y. 1984b. Sexually dimorphic radulae in Cronia mar-
gariticola and Morula musiva (Gastropoda: Muricidae). Ve-
nus 43:315-330.

Fujioka, Y. 1985. Seasonal aberrant radular formation in Thais
bronnt (Dunker) and 7. clavigera (Kuster) (Gastropoda:
Muricidae). Jour. Exp. Mar. Biol. Ecol. 90:43-54.

GRAHAM, A. 1965. The buccal mass of ianthinid prosobranchs.
Proc. Malacol. Soc. Lond. 36:323-338.

HICKMAN, C. S. 1980. Gastropod radulae and the assessment
of form in evolutionary paleontology. Paleobiology 6:276-
294.

HOLLISTER, S. C. 1954. Some notes on the radula. Nautilus
68:44-46.

KEEN, A. M. 1971. Sea shells of tropical west America. 2nd
ed. Stanford Univ. Press: Stanford, California. 1064 pp.

Locn, I. 1982. Queensland epitoniids. Aust. Shell News 39:
3-6.

Luna, L.G. 1968. Manual of histologic staining of the armed
forces institute of pathology. 3rd ed. McGraw-Hill Book Co.:
New York. 258 pp.

MacLeisH, K. 1973. Exploring Australia’s coral jungle. Natl.
Geogr. Mag. 143:743-778.

McLean, J. H. & J. NYBAKKEN. 1979. On the growth stages
of Conus fergusoni Sowerby, 1873, the reinstatement of Conus
xanthicus Dall, 1910, and a new species of Conus from the
Galapagos Islands. Veliger 22:135-144.

MELONE, G. 1986. Sex changes in Opalia crenata (L.) (Gas-
tropoda: Epitoniidae). Abstracts, Ninth Int. Malacol. Con-
gress, Edinburgh, 1986: 54 (abstract only).

MIKKELSEN, P. S. 1985. A rapid method for slide mounting of
minute radulae, with a bibliography of radula mounting
techniques. Nautilus 99:62-65.

NISHIWAKI, S. 1964. Phylogenetical study on the type of the
dimorphic spermatozoa in Prosobranchia. Sci. Rept. Tokyo
Kyoiku Daigaku Sect. B. 11:237-275.

NISHIWAKI, S. & T. TOCHIMOTO. 1969. Dimorphism in typical
and atypical spermatozoa forming two types of spermato-
zeugmata in two epitoniid prosobranchs. Venus 28:37-46,
2 pls.

NYBAKKEN, J. 1970. Radular anatomy and systematics of the
west American Conidae (Mollusca, Gastropoda). Amer. Mus.
Novit. 2414:1-29.

NYBAKKEN, J. 1981. Ontogenetic change in the molluscan rad-
ula, some cases from the genus Conus. Bull. Amer. Malacol.
Union 1981:28 (abstract only).

ROBERTSON, R. 1970. Review of the predators and parasites
of stony corals, with special reference to symbiotic proso-
branch gastropods. Pacific Sci. 24:43-54.

ROBERTSON, R. 1981. Protandry with only one sex change in
an Epitonium (Ptenoglossa). Nautilus 95:184-186.

ROBERTSON, R. 1985. Archaeogastropod biology and the sys-
tematics of the genus Tricolia (Trochacea: Tricoliidae) in the
Indo-West-Pacific. Monogr. Mar. Mollusca 3:1-103.

ROBERTSON, R. & P. L. ScHUTT. 1984. Golden wentletraps
on golden corals. Hawaiian Shell News 32:1, 4.

RupMaNn, W. B. 1984. Molluscs. Pp. 172-197. In: Reader’s
Digest book of the Great Barrier Reef. Reader’s Digest:
Sydney.

A. J. Page & R. C. Willan, 1988

STERKI, V. 1893. Growth changes of the radula in land-mol-
lusks. Proc. Acad. Natur. Sci. Phila. 1893:388-400, pls. 10,
Ie

Taki, I. 1956. Anatomical study on Japanese Epitoniidae (1)
Epitonium, Amaea and Papyriscala. Bull. Natur. Sci. Mus.
(Tokyo) 3:71-79, pls. 13-17.

Taki, I. 1957. Anatomical study on Japanese Epitoniidae (2)
Gyroscala and Acutiscala. Bull. Natur. Sci. Mus. (Tokyo) 3:
176-182, pls. 34-38.

THIELE, J. 1928. Uber ptenoglosse Schnecken. Z. Wiss. Zool.
132:73-94.

Page 229

THOMPSON, T. E. 1958. Observations on the radula of Adalaria
proxima (A. & H.) (Gastropoda, Opisthobranchia). Proc.
Malacol. Soc. Lond. 33:49-56.

TuHompson, T. E. & G. BROWN. 1984. Biology of opisthobranch
molluscs. Vol. II. The Ray Society: London. 229 pp.

TocHIMoTO, T. 1967. Comparative histochemical study on the
dimorphic spermatozoa of the Prosobranchia with special
reference to polysaccharides. Sci. Rept. Tokyo Kyoiku Dai-
gaku Sect. B. 13:75-109.

The Veliger 30(3):230-243 (January 4, 1988)

THE VELIGER
© CMS, Inc., 1988

Illustrated Embryonic Stages of the Eastern

Atlantic Squid Loligo forbes

by

S. SEGAWA,' W. T. YANG, H.-J. MARTHY,? AnD R. T. HANLON

The Marine Biomedical Institute, The University of Texas Medical Branch,
200 University Boulevard, Galveston, Texas 77550, U.S.A.
"Tokyo University of Fisheries, Minato-Ku, Konan-cho, Tokyo 108, Japan
* Universite Pierre et Marie Curie, Biologie Marine, Laboratoire Arago,
66650 Banyuls-sur-Mer, France

Abstract.

The embryonic development of Loligo forbes: was observed from 14-day-old eggs to natural

hatching. Egg strands were spawned in floating cages by wild-caught females in the Azores Islands,
air-shipped to Galveston, and incubated in a closed seawater system. The period from spawning to
hatching ranged from 68 to 75 days at a mean temperature of 12.5°C (SD 0.5°C). The diameters of
individual eggs ranged from 3.0 to 3.1 mm and the dorsal mantle lengths of hatchlings ranged from 4.3
to 4.9 mm. The major developmental patterns were nearly identical to those of L. vulgaris (eastern
Atlantic Ocean) and L. peale: (western Atlantic Ocean), except that L. forbes: took longer to hatch
because of the larger embryos and hatchlings. The most noticeable differences in development involved
the number and distribution of chromatophores. The chromatophore pattern was one of the best criteria

for staging L. forbes: in late development.

INTRODUCTION

Loligo forbesi Steenstrup, 1856, is an eastern Atlantic Ocean
species distributed from about 60°N on the coast of Norway
to 20°N on the coast of northwest Africa (ROPER et
al., 1984) and throughout the Mediterranean Sea
(MANGOLD-WIRZ, 1963). It is one of the economically im-
portant species in the English Channel (HOLME, 1974),
in Scottish waters (THOMAS, 1973), in the Azores Islands
(MarTINS, 1982), and off Spain and France (WORMS,
1983a). Studies to date on this species have been primarily
of a taxonomic nature (ADAM, 1955) or works concerned
mainly with aspects of fisheries biology (HOLME, 1974;
MarTINS, 1982). Embryological observations are limited
to a short note by NAEF (1928) comparing L. forbes: to L.
vulgaris.

This embryological study was undertaken primarily to
help predict the onset of hatching in laboratory growth
studies (e.g., YANG et al., 1980; BOLETZKY & HANLON,
1983; HANLON et al., 1985). Loliginid squids are important
for biomedical experimentation (e.g., NIXON & MEs-
SENGER, 1977; TANSEY, 1979), especially the giant fibers
of the peripheral nervous system (ADAMS ef al., 1983).
Loligo forbesi is a particularly promising species to culture
because of its large hatchling size (HANLON et al., 1985).

The present paper illustrates the morphological form of
post-cleavage stages in the embryonic development of Lo-
ligo forbesi. Criteria established by NAEF (1928) for L.
vulgaris and ARNOLD (1965) for L. peale: have been used
in conjunction with our observations of several additional
characters, namely chromatophore pattern development
(cf. FIORONI, 1965) and internal organ formation.

MATERIALS anD METHODS

Egg capsules were laid 28 January 1986 by captive adult
female Loligo forbes: caught with squid jigs at a depth of
200 m near the island of Faial in the Azores Islands. The
females laid their eggs in a large floating cage (2 x 3 x
2 m) in Horta harbor on Faial where the local water
temperature was 14 to 16°C and the salinity 36%. Live
embryos were transported by air freight from the Azores
to the Marine Biomedical Institute 11 days after spawning.
Twenty-two strands of eggs were shipped in two plastic
bags containing about 5 L of seawater and an equal volume
of oxygen at temperatures of 12 to 15°C. Upon arrival the
eggs were acclimated gradually to the conditions of the
closed recirculating tank system. The egg capsules were
suspended in the water column and incubated at a salinity
of 34 to 35% and a mean temperature of 12.5°C (SD
0.5°C).

S. Segawa et al., 1988

30

25

20

15

10

Arnold (1965) stages e

O 10 20 30

Page 231

Naef (1928) stages o

40 50 60 70

Days after spawning
Figure 1

Embryonic development of Loligo forbes: in comparison to the stages proposed by ARNOLD (1965) and NAEF (1928)
during the period from 14-day-old embryo to hatching. (Mean incubation temperature 12.5°C; SD 0.5°C.)

Regular observations were made from 14-day-old eggs
throughout the remainder of embryonic development on
four egg strings with embryos of uniform age. Represen-
tative embryos were observed carefully and drawn to scale
under a dissecting microscope. All drawings were made
from living embryos. In the early stages before organo-
genesis, embryos were observed through the chorion after
careful removal of the tunic, and in older ones observations
were made after removal of the chorion. The arabic stage
represents the stage proposed by ARNOLD (1965) and the
Roman numeral stage represents the stage proposed by
NAEF (1928). Both ventral and dorsal views are given after
stage 26 (XIV) (Figure 19); before that the dorsal view
did not add substantially more information. Chromato-
phores on the fins were included in the “dorsal mantle”
counts.

RESULTS

The egg capsules were transparent, soft, gelatinous, and
fingerlike in shape. At the beginning of our observations
(14 days after spawning), the eggs were stage 12 according
to ARNOLD’s (1965) scheme and stage II+ by NAEF’s (1928)
scheme, and each egg capsule was approximately 18 cm

long and contained about 85 to 100 eggs arranged in a
spiral. The diameters of the embryos ranged from 3.0 to
3.1 mm. From egg laying to day 14 in the Azores Islands,
the environmental conditions were only moderately con-
stant in the harbor for 11 days and during the 36 h of
transportation to the U.S.A. The embryos took 68 to 75
days to hatch at 12.5 + 0.5°C, with the main hatch on
days 69 and 70. Figure 1 shows the developmental time
of Loligo forbes: from day 14 to hatching according to the
developmental stages of both ARNOLD (1965) and NAEF
(1928).

Pre-organogenesis: Germ Layer Formation

Figure 2: Stage 12, Arnold (1965); (Stage II+), Naef
(1928): Formation of the germ layer, or “gastrulation,” is
a complex process that begins when the margin of the
blastoderm becomes two-layered as described in Loligo
pealer (SINGLEY, 1977) and L. vulgaris (MARTHY, 1982),
and the radial arrangement of blastocones becomes streaked.
The definite separation of the blastoderm into an ectoder-
mal and a mesendodermal germ layer is accomplished
during stages 12-13 (III).

Page 232

Pre-organogenesis: Germ Layer Proliferation
(Blastoderm Growing)

Figure 3: Stage 13— (III-IV): Blastoderm covers 10 to
20% of the egg length, and border of blastoderm becomes
sharply distinct.

Figure 4: Stage 13 (IV): Blastoderm covers about one-
third of the egg surface.

Figure 5: Stage 14 (V): Blastoderm covers about one-half
of the egg.

Figures 6 and 28: Stage 15 (VI): Blastoderm covers three-
fifths to two-thirds of the egg.

Figure 7: Stage 15+ (VI-VII): Blastoderm covers about
four-fifths of the egg. A shallow girdling depression ap-
pears around the equator forming a boundary between the
future external yolk sac and the future embryonic body.
The chorion is not illustrated in this and following figures.

Organogenesis

Figure 8: Stage 16 (VII), lateral view: Outer yolk sac
envelope nearly closed. Primordia of optic vesicles are ru-
dimentary and visible as disc-like elevations. Primordium
of shell gland now visible.

Figure 9: Stage 17 (VII-VIID), lateral view: Outer yolk
sac envelope closed. A ridge of the disc-like elevation trans-
forms into a fold in the ventral area and forms a ridge in
the dorsal part that becomes the optic vesicle. Border of
the shell gland elevated slightly. Primordia of arms and
tentacles first visible.

Figure 10: Stage 18 (VIII), lateral view: The disc-like
fold entirely surrounds prospective retina and starts grow-
ing over it. Primordia of statocysts appear. Arms and ten-
tacles grow and begin to project.

Figure 11: Stage 19 (VIII-IX), ventral view: Closure of
the optic vesicle is progressing. Other organ primordia
become prominent, such as gills and anal knoll.

Figure 12: Stage 20 (IX), ventral view: Opening of the
optic vesicle closes. Shell gland invagination is progressing.
Posterior and anterior funnel folds extend towards the
midline.

The Veliger, Vol. 30, No. 3

Figure 13: Stage 21 (X), ventral view: Shell gland com-
pletely closes and transverse fin folds develop upon the
broadening mantle. Anterior and posterior funnel folds
fuse together. Funnel folds on each side elevate clearly but
fusion in midline has not begun. First suckers appear on
tentacles.

Figure 14: Stage 22 (XI), ventral view: Anterior part of
funnel fold comes together at the margin. Lens primordia
first visible. Mantle covers one-half to two-thirds of gills.
Suckers appear on arms III. Retina pigmentation begins.

Figures 15 and 29: Stage 23 (XI-XII), ventral view:
Funnel fold fuses anteriorly. Statocysts completely formed.
Lenses are evident as refractive rods. Gills segmented clear-
ly, showing six pairs of leaflets.

Figure 16: Stage 24 (XII), ventral view: Funnel tube
closed. Mantle covers the anal papilla and gills but funnel
retractor muscle is still visible.

Figure 17: Stage 25 (XIII), ventral view: Mantle covers
the posterior portion of the funnel but triangular opening
is still evident. Systemic heart clearly visible. Bases of arms
IV and tentacles start to extend. Posterior lobes of internal
yolk sac increase in size. First yellow chromatophores ap-
pear on the ventral mantle.

Figure 18: Stage 25+ (XIII+), ventral view: Mantle
completely covers the posterior margin of the funnel. Ven-
tral mantle chromatophores increase in number. First
chromatophores are visible on tentacles; these appear to
be dark reddish from the beginning.

Figure 19: Stage 26 (XIV), dorsal (left) and ventral
(right) views: Ventral arm bases (the ventral component
of the future primary lid) cover about one-half of the optic
ganglia. Ink sac is first visible but no ink is present. Retina
color is brilliant reddish. Chromatophores are first visible
on the ventral and dorsal sides of head, the dorsal mantle
and fins, and the fourth arms.

Figure 20: Stage 27 (XVI), dorsal (left) and ventral
(right) views: Ventral arm bases extend into a primary
lid and the edge reaches posterior end of eye vesicle. Ink
sac fills with ink. Anus structure clearly visible with con-
spicuous anal papillae or flaps.

Explanation of Figures 2 to 27

Embryonic development of Loligo forbesi, from germ layer formation to newly hatched squid. See Results for details
of each Figure. Key to abbreviations: a, anal knoll; ap, anal papilla or flaps; bd, blastoderm; bh, branchial heart;
bu, buccal mass; c, caecum; ch, chorion; co, cornea; d, dark reddish chromatophore; ft, funnel tube; g, gill; h, Hoyle’s
Organ; is, ink sac; ly, internal yolk; 1, lens; m, mantle; mg, mid-gut gland; 0, optic vesicle; og, optic ganglion; op,
olfactory plate; pa, primordia of arms; paf, primordium of anterior funnel fold; pf, primordium of fin; pg, primordium
of gill; pl, primordium of lens; pm, primordium of mantle; po, primordium of optic vesicle; ppf, primordium of
posterior funnel fold; psg, primordium of shell gland; pst, primordium of statocyst; py, posterior lobes of internal
yolk sac; sg, shell gland; sh, systemic heart; sm, stomach; st, statocyst; su, sucker; y, yellow chromatophore; yo, yolk;
Al, arm I; A2, arm II; A3, arm III; A4, arm IV; T, tentacle; HD, dorsal side of head; HV, ventral side of head;

MD, dorsal side of mantle; MV, ventral side of mantle.

S. Segawa et al., 1988 Page 233

The Veliger, Vol. 30, No. 3

Page 234

Total 48

Total 64

S. Segawa et al., 1988

Figure 21: Stage 27+ (XVII), dorsal (left) and ventral
(right) views: The edge of the primary lid covers about
one-half of eye vesicle. Hoyle’s organ is first visible on
dorsal mantle. Chromatophores on arms II first appear.

Figure 22: Stage 28 (XVIII), dorsal (left) and ventral
(right) views: Primary lid completely covers the optic ves-
icle and part of it transforms into a transparent cornea.

Page 235

Q| 2
HV d 12

MV y 10
d 37

Total 75

External yolk sac approximately same size as mantle length.
Second row of chromatophores appears on the tentacles;
these begin as yellows.

Figure 23: Stage 28+ (XVIII-XIX), dorsal (top) and
ventral (bottom) views: Mid-gut gland first visible around
the internal yolk sac. Stomach and caecum first visible.

The Veliger, Vol. 30, No. 3

Page 236

| a)
WwW
©
we
fo)
fe

S. Segawa et al., 1988

AQ id * 2
A3 y 2
HD y 4
d 11
MD y 17
d 30
Total 66
ee

A4 y 2
d 4

le 2 iV «eda
d 20

HV y 3
(fat) PA

MV y 16
d 47

Total 115

Page 237

Page 238 The Veliger Viol 0 Nowe

Qaa< a
BNMN ND

y
fo el
y
d 34
Total 98

d
y 14
d 28

HV y 7
el 2

MV y 26
d 50

Total 143

Page 239

S. Segawa ef al., 1988

<e)
=
=_-

ie)
=
o}
=

Total 154

Page 240 The Veliger, Vol. 30, No. 3

MD y 33

12
33

12
13

27
54

Total 159

<=
<
(yg fe ESS (el

S. Segawa et al., 1988

28 29

Page 241

Explanation of Figures 28 to 30

Figure 28. Photograph of embryo at stage 15 (VI). Compare
Figure 6.

Figure 29. Photograph of embryo at stage 23 (XI-XII). Compare
Figure 15.

Figures 24 and 30: Stage 29 (XIX), dorsal (top) and
ventral (bottom & Figure 30) views: Third row of chro-
matophores appears on tentacles; these are small and red
from the start. First chromatophores appear on arms III.
The primordia of the olfactory organ are clearly visible on
the ventral head as thickenings of the epidermis.

Figure 25: Stage 29+ (XIX+), dorsal (top) and ventral
(bottom) views: Internal yolk sac begins to be absorbed
and decreases in size. Mid-gut gland develops around the
internal yolk sac. The external yolk sac approximately
equal in length to tentacle length. First chromatophores
and suckers appear on arms II.

Figure 26: Stage 29++ (XIX-XX), dorsal (top) and
ventral (bottom) views: The external yolk sac is approx-
imately equal to length of arms II. Internal yolk sac re-
duced in size. Caecum and stomach increase in size. In
some embryos, the external yolk sac may be lost and pre-
mature hatching may occur. Dark chromatophore patterns
on both dorsal and ventral head remain the same until
hatching.

Figure 30. Photograph of embryo at stage 29 (XIX). Compare
Figure 24.

Figure 27: Stage 30 (XX), dorsal (top) and ventral (bot-
tom) views: Newly hatched squid. Hoyle’s organ depleted.
Internal yolk sac visible dorsally and reduced to a small
triangular body. External yolk almost absorbed and only
yolk sac envelope remains. External yolk sac sometimes
lost just after hatching. Hatching size ranged from 4.3 to
4.9 mm ML, with a mean of 4.6 mm ML (SD 0.1 mm).

DISCUSSION

The life history of Loligo forbes: is known only in general
terms (e.g., HOLME, 1974; MARTINS, 1982) and this study
plus our laboratory culture experiments (e.g., HANLON et
al., 1985) are meant to fill some of the gaps. Details of
development may also help distinguish L. forbes: from the
closely related L. vulgaris, with which it shares many mor-
phological features and also overlaps in distribution (ROPER
et al., 1984).

For embryological study, among the best-known ceph-
alopods are Loligo vulgaris and L. pealei, for which detailed
staging schemes were established by NAEF (1928) and
ARNOLD (1965) respectively. Although there are some dif-

Page 242

ferences in developmental processes between these two
species and L. forbesi, Arnold’s and Naef’s schemes could
be transferred directly to the developmental sequence of
L. forbesu.

The sigmoid developmental pattern of Loligo forbes:
(Figure 1) was very similar to other species of Loligo
(BOLETZKY, 1974:fig. 1) but a little different from that
reported for L. peale: (ARNOLD, 1965), whose development
after stage 12 was approximately linear. Loligo forbes: has
large eggs that are deposited in cold water. Individual eggs
of L. forbest spawned in the Azores were 3.0-3.1 mm in
diameter and represent the largest known egg of Loligo
spp.: L. opalescens 2.0-2.5 mm (FIELDS, 1965), L. vulgaris
2.3-2.7 mm (WoRMS, 1983b), and L. peale: 1.0-1.6 mm
(SUMMERS, 1983). As a result, the eggs develop more slow-
ly than other Loligo species. It took 68-75 days at 12.5°C
for L. forbest compared to 10-27 days at 12-23°C for L.
pealer. (MCMAHON & SUMMERS, 1971), 30-35 days at
13.6°C for L. opalescens (McGowan, 1954), and 45-70
days at 12-14°C for L. vulgaris (MANGOLD-WIRZ, 1963;
BOLETZKY, 1974).

Development is a continual process, but the develop-
mental “stages” have been determined arbitrarily. Thus,
identification of a particular stage is sometimes difficult.
In each case several stages are divisible into two or more
steps. The “ideal” staging criteria suggested by NAEF
(1928), and partially reconsidered by ARNOLD (1965, 1974),
follow morphological events throughout embryogenesis (e.g.,
easily recognizable steps in eye and shell gland closure,
funnel formation, eye lid growth, etc.) and are useful in
Loligo forbest as well. Progressive closure of the optic ves-
icle, as described for L. vulgaris (MARTHY, 1973) and L.
peale:. (ARNOLD & WILLIAMS-ARNOLD, 1978), is a good
indicator for stages 16-20 (VII-IX). The process of funnel
folding (ARNOLD et al., 1978) and of formation of the
primary lid over the eye (NAEF, 1928; ARNOLD, 1984) are
excellent criteria for stages 20-24 (IX-XII) and stages
25-28 (XIII-X VIII) respectively. The proportions among
some internal organs such as internal yolk sac, mid-gut
gland, stomach, caecum, and ink sac change rapidly from
stages 28 to 30 (XVIII to XX), but their size and position
are good staging criteria.

We distinguish yellow from dark chromatophores be-
cause nearly all chromatophores in the embryo begin as
yellows and transform into a darker (red-brown) pigment
with time (e.g., FIORONI, 1965; FORSYTHE & HANLON,
1985; PACKARD, 1985). This progression can be seen in
the figures and is useful in staging. The third (inner) row
of chromatophores to form on the tentacles at stage 29
(XIX) (Figure 24) are an exception; they start as dark
reddish and are conspicuously smaller chromatophore or-
gans, and this appears to be characteristic of Loligo spp.
hatchlings (e.g., FIORONI, 1965; MCCONATHY et al., 1979).
There appears to be no “standard color” of the dark chro-
matophores at hatching; unpublished data of Hanlon and
Boletzky show that some year-classes of L. forbesi have
red, and some have brown, dark chromatophores. Thus,

The Veliger, Vol. 30, No. 3

color alone is not useful in characterizing the species; fur-
thermore, in preservation the colors are not usually dis-
tinguishable.

In Loligo forbesi, chromatophores on the ventral surface
appear at stage 25 (XIII) (Figure 17) and on the dorsal
surface at stage 26 (XIV) (Figure 19). These are earlier
than those of L. peale: (ARNOLD, 1965) and later than
those of L. vulgaris (FIORONI & MEISTER, 1974). After
first appearance, chromatophores increase in number and
distribution on the head, mantle, fins, arms, and tentacles.
The chromatophores (especially the dark reddish ones that
are easier to see) on the head, tentacles, and arms are one
of the best criteria for determining later developmental
stages in L. forbes:. There is considerable variation in the
pattern of chromatophores on the mantle; thus the use of
mantle chromatophores in distinguishing this species from
the sympatric L. vulgaris will be minimal.

Size of Loligo forbes: at hatching ranges from 4.3 to 4.9
mm ML and is larger than other species such as L. pealez
(about 1.8 mm ML; McConatny et al., 1979), L. vulgaris
(about 3 mm ML; BOLETzky, 1979), and L. opalescens
(2.5-3.2 mm ML; FIELDs, 1965; MCCONaATHY et al., 1979).
Size of hatchlings depends largely upon the size of eggs
spawned. In laboratory experiments (unpublished obser-
vations), larger hatchlings of squids like L. forbes: usually
have more successful attacks on food organisms and have
better survival rates than smaller hatchlings like L. pealez.
This suggests that L. forbes: has a different way of optimiz-
ing survival during its initial life-history stages: the large
hatchlings are already a size that takes other Loligo hatch-
lings several weeks to attain, and they can feed immediately
on a wide size range and diversity of food organisms (from
approximately 0.8 mm to 3.5 mm long; Hanlon et al.,
submitted). Thus, it should be relatively easier to rear L.
forbesi in captivity during the first critical month (e.g.,
YANG et al., 1986) when mortality is generally very high.

ACKNOWLEDGMENTS

S. Segawa thanks the Ministry of Education, Science
and Culture of Japan and The Marine Biomedical Insti-
tute for funding during his postdoctoral study at The Uni-
versity of Texas Medical Branch in Galveston. We grate-
fully acknowledge funding for work in the Azores and
Galveston on DHHS grant RR 01024 to R.T.H. and
W.T.Y. John W. Forsythe did a superb job of acquiring
the eggs in the Azores and transporting them, and we thank
Dr. Jose Martins, Dr. Helen Rost Martins, and Ricardo
de Santis of the University of the Azores for hospitality
and assistance with squid work in the Azores. We thank
Dr. John Arnold for reviewing a late draft and especially
Dr. Sigurd Boletzky for many detailed suggestions on the
final draft. Laura A. Koppe kindly typed the drafts and
final manuscript.

LITERATURE CITED

ADAM, W. 1955. Résultats scientifiques des campangnes de la

“Calypso.” I. Campagne en Mer Rouge. VI. Cephalopodes.
Annales Institut Oceanographique 30:185-195.

S. Segawa et al., 1988

Page 243

ADAMS, D. J., K. TAKEDA & J. A. UMBACH. 1983. Metabolic
inhibitors and lithium depress synaptic transmission at the
squid giant synapse. Jour. Physiol. 345:147 pp.

ARNOLD, J. M. 1965. Normal embryonic stages of the squid,
Loligo pealu (Lesueur). Biol. Bull. 128:23-32.

ARNOLD, J. M. 1974. Embryonic development. Pp. 24-49. In:
J.M. Arnold, W. C. Summers, D. L. Gilbert, R. S. Manalis,
N. W. Daw & R. J. Lasek (eds.), A guide to laboratory use
of the squid Loligo peale:. Marine Biological Laboratory:
Woods Hole, Massachusetts.

ARNOLD, J. M. 1984. Closure of the squid cornea: a muscular
basis for embryonic tissue movement. Jour. Exper. Zool.
232:187-195.

ARNOLD, J. M. & L. D. WILLIAMS-ARNOLD. 1978. Preliminary
studies on the closure of the optic vesicle of Loligo pealei
embryos. Biol. Bull. 155:426 (abstract).

ARNOLD, J. M., L. D. WILLIAMS-ARNOLD & V. PETERS. 1978.
Fusion of tissue masses in embryogenesis—a scanning elec-
tron microscope and transmission electron microscope study
of funnel development in the squid Loligo pealei. Develop.
Biol. 65:155-170.

BOLETZKY, S. v. 1974. The larvae of Cephalopoda: a review.
Thalassia Jugosl. 10(1/2):45-76.

BOLETZKY, S. v. 1979. Observations on the early post-embry-
onic development of Loligo vulgaris (Mollusca, Cephalopo-
da). Rapport de la Commission Internationale Pour la Mer
Mediterranee 25/26(10):155-158.

BoLeTzky, S. v. & R. T. HANLON. 1983. A review of the
laboratory maintenance, rearing and culture of cephalopod
molluscs. Mem. Natl. Mus. Victoria 44:147-187.

FIELDS, W. G. 1965. The structure, development, food rela-
tions, reproduction and life history of the squid Loligo opa-
lescens Berry. Calif. Dept. Fish & Game, Fish. Bull. 131:
1-108.

FIoRONI, P. 1965. Die embryonale Musterentwicklung bei ei-
nigen Mediterranean Tintenfischarten. Vie et Milieu, Serie
A: Biologie Marine 16:654-756.

Froroni, P. & G. MEISTER. 1974. Embryologie von Loligo
vulgaris Lam. Gemeiner Kalmar. Gustav Fischer Verlag:
Stuttgart. Grosses Zoologisches Praktikum, Heft 16 c/2. 69

PP-

ForsyTHE, J. W. & R. T. HANLON. 1985. Aspects of egg
development, post-hatching behavior, growth and reproduc-
tive biology of Octopus burry: Voss, 1950 (Mollusca, Ceph-
alopoda). Vie et Milieu 35(3/4):273-282.

HANLON, R. T., R. F. Hixon, P. E. Turk, P. G. LEE & W. T.
YANG. 1985. Behavior, feeding and growth of young Loligo
forbest (Cephalopoda: Myopsida) reared in the laboratory.
Vie et Milieu 35(3/4):247 (abstract).

HANLON, R. T., W. T. YANG, P. E. Turk, P. G. LEE & R. F.
HIxon. Submitted. Laboratory culture of the eastern At-
lantic squid Loligo forbesi. Aquaculture and Fisheries Man-
agement.

Home, N. A. 1974. The biology of Loligo forbesi Steenstrup
(Mollusca: Cephalopoda) in the Plymouth area. Jour. Mar.
Biol. Assoc. U.K. 54:481-503.

MANGOLD-WIRZ, K. 1963. Biologie des Cephalopodes benthi-
ques et nectoniques de la Mer Catalane. Vie et Milieu,
Suppl. No. 13:285 pp.

MartTuy, H.-J. 1973. An experimental study of eye devel-
opment in the cephalopod Loligo vulgaris: determination and
regulation during formation of the primary optic vesicle.
Jour. Embryol. Exper. Morphol. 29:347-361.

Martny, H.-J. 1982. The cephalopod egg, a suitable material
for cell and tissue interaction studies. Pp. 223-233. In: M.
M. Burger & R. Weber (eds.), Progress in clinical biological
research. Vol. 85. Allan R. Liss Publishers: New York.

MarTINS, H.R. 1982. Biological studies of the exploited stock
of Loligo forbes: (Mollusca: Cephalopoda) in the Azores.
Jour. Mar. Biol. Assoc. U.K. 62:799-808.

McConatny, D. A., R. T. HANLON & R. F. Hixon. 1979.
Chromatophore arrangements of hatchling loliginid squids
(Cephalopoda, Myopsida). Malacologia 19(2):279-288.

McGowan, J. A. 1954. Observations on the sexual behavior
and spawning of the squid, Loligo opalescens, at La Jolla,
California. Calif. Dept. Fish & Game 40:47-54.

McManon, J. & W. C. SUMMERS. 1971. Temperature effects
on the developmental rate of squid (Loligo peale:) embryos.
Biol. Bull. 141:561-567.

NaF, A. 1928. Die Cephalopoden. Fauna Flora Golf Neapal
35(II):357 pp.

Nixon, M. & J. B. MESSENGER. 1977. The biology of ceph-
alopods. Symposia of the Zoological Society of London, No.
38. Academic Press: London. 615 pp.

PACKARD, A. 1985. Sizes and distribution of chromatophores
during post-embryonic development in cephalopods. Vie et
Milieu 35(3/4):285-298.

Roper, C. F. E., M. J. SWEENEY & C. E. NAUEN. 1984. Ceph-
alopods of the world: an annotated and illustrated catalogue
of species of interest to fisheries. FAO Fisheries Synopsis
3(125):277 pp.

SINGLEY, C. T. 1977. An analysis of gastrulation in Loligo
peale:. Ph.D. Thesis, University of Hawaii, Honolulu.
SUMMERS, W. C. 1983. Loligo pealer. Pp. 115-142. In: P. R.
Boyle (ed.), Cephalopod life cycles. Vol. I: Species accounts.

Academic Press: London.

TANSEY, E. M. 1979. Neurotransmitters in the cephalopod
brain. Comp. Biochem. Physiol. 64C:173-182.

Tuomas, H. J. 1973. Squid. Scottish Fisheries Bulletin 39:
35-39.

Worms, J. 1983a. World fisheries for cephalopods: a synoptic
overview. FAO Fisheries Technical Papers (231):1-20.
WorMsS, J. 1983b. Loligo vulgaris. Pp. 143-157. In: P. R. Boyle
(ed.), Cephalopod life cycles. Vol. I: Species account. Aca-

demic Press: London.

YANG, W. T., R. T. HANLON, R. F. HIXON & W. H. HULET.
1980. First success in rearing hatchlings of the squid Loligo
pealei Lesueur, 1821. Malacol. Rev. 13:79-80.

YANG, W. T., R. F. Hixon, P. E. Turk, M. E. Krejci, W. H.
Huet & R. T. HANLON. 1986. Growth, behavior, and
sexual maturation of the market squid, Loligo opalescens,
cultured through the life cycle. Fish. Bull. 84(4):771-798.

The Veliger 30(3):244-247 (January 4, 1988)

THE VELIGER
© CMS, Inc., 1988

The Red Foot of a Lepidopleurid Chiton:

Evidence for Tissue Hemoglobins

DOUGLAS J. EERNISSE!

Friday Harbor Laboratories, University of Washington,
Friday Harbor, Washington 98250, U.S.A.

NORA B. TERWILLIGER AnD ROBERT C. TERWILLIGER

Department of Biology, University of Oregon, Eugene, Oregon 97403, U.S.A. and
Oregon Institute of Marine Biology, Charleston, Oregon 97420, U.S.A.

Abstract. Shallow-water specimens of Leptochiton rugatus, a member of an ancient, mostly deep-
water, suborder of chitons (Lepidopleurina), have a striking red coloration of the foot and soft tissues.
The possibility that the red color of various tissues of L. rugatus is caused by a circulating or noncirculating
respiratory heme protein was investigated. A hemoglobin was identified in tissue from foot, mantle wall,
gills, and surrounding the mouth. No heme protein was found in circulating hemolymph; rather a
hemocyanin is likely present. It is hypothesized that the presence of this tissue hemoglobin might somehow
facilitate O, transport in the shallow, hypoxic habitat of this animal.

INTRODUCTION

Among the diverse chiton fauna on the shores of western
North America, a single species of the suborder (or order)
Lepidopleurina Thiele, 1910, Leptochiton rugatus (Car-
penter in Pilsbry, 1892), is occasionally encountered in
fair numbers living in shallow water, usually on the un-
derside of large submerged rocks at low tide. Members of
the Lepidopleurina, referred to collectively here as “‘lep-
idopleurid” chitons, are generally considered the most
primitive of our living chitons based on their general lack
of well developed and slitted insertion plates (usually in
all eight valves), their gills which are few in number and
placed posteriorly, and their unspecialized tegmentum and
girdle features (KAAS & VAN BELLE, 1985). Fossil data
also support this conclusion. Over 50 fossil lepidopleurid
species are known from the Paleozoic and Mesozoic eras
(VAN BELLE, 1981) and, of these, one is possibly a Lep-
tochiton, L. deshayesi (Terquem, 1852) reported from the

' Send reprint requests to D.J.E. at Museum of Zoology and
Department of Biology, University of Michigan, Ann Arbor,
Michigan 48109, U.S.A.

lower Jurassic period of the Mesozoic. In contrast, species
assigned to other extant families are unknown from the
Paleozoic and number fewer than 10 species from the
Mesozoic (VAN BELLE, 1981; HOARE & SMITH, 1984).
.As in other groups with some ancient members, the
primitive lepidopleurids seem to have persisted primarily
in deep waters and have been collected from depths ex-
ceeding 7000 m (review by FERREIRA, 1979). The absence
of lepidopleurids in exposed intertidal habitats may reflect
a fundamentally different functional arrangement of gills.
Based on observations of actively respiring animals, YONGE
(1939) argued that the posterior gill arrangement in the
lepidopleurid species Leptochiton asellus was less efficient
for aerial respiration than the more anterior gill placement
of three modern chiton species he examined. Although
Yonge based his conclusions on relatively few species, his
generalities concerning the morphological and habitat dif-
ferences between lepidopleurids and modern chitons are
probably valid, judging from reviews of gill arrangements
and collection depths of more than 200 chiton species by
EERNISSE (1984, 1985) and Kaas & VAN BELLE (1985,
1986). Yonge proposed that the innovation in gill arrange-
ment by modern chitons led to the replacement of lepi-
dopleurids in the intertidal. As discussed by EERNISSE

D. J. Eernisse et al., 1988

(1984), it is equally plausible that lepidopleurids never
were able to colonize intertidal habitats, given their pos-
terior gill placement. It is interesting, therefore, that L.
rugatus can occur in shallow depths as well as in deeper
waters (specimens identified as L. rugatus have been dredged
from a depth of about 458 m). If most lepidopleurids are
to some extent limited to deeper water by their gill mor-
phology, the shallow habitat of L. rugatus may indicate a
special adaptation to shallow water conditions.

It was with the unusual shallow-water habitat in mind
that we noted the distinctive red coloration of the foot, gills,
and other soft parts on the underside of Leptochiton rugatus.
As far as we know, this condition is peculiar to L. rugatus,
and may be peculiar to only shallow-water specimens of
L. rugatus (R. N. Clark, personal communication). It is
also our experience that L. rugatus tends to occur in locally
dense populations on the bottoms of large rocks submerged
in oxygen-poor mud. This study investigates the possibility
that the red coloration of the soft parts of L. rugatus is
caused by a circulating or noncirculating respiratory heme
protein which might somehow facilitate respiration in shal-
low, oxygen-poor habitats.

MATERIALS anpD METHODS

Leptochiton rugatus was collected intertidally in May 1986
on the western shores of San Juan Island, Washington,
U.S.A. (48°03'N, 123°05'W), and animals were identified
according to FERREIRA (1979). The animals studied mea-
sured about 6.5-8.0 mm in length.

Ten animals were dissected. An incision was made in
the mantle cavity near the gills and a very small amount
of hemolymph was collected from each animal. The foot
and surrounding mantle tissue were then removed and
homogenized in cold phosphate buffer (0.5 M NaCl, 0.05
M sodium phosphate buffer, pH 7.5) in a scintered glass
micro-homogenizer. Radular muscles were extracted in the
same manner. Animal hardparts were flattened and pre-
served in 70% ethanol as voucher specimens (D JE coll.).
Homogenates and blood samples were centrifuged at 13,000
g for 2 min and supernatants were used in the following
studies.

Samples were electrophoresed on a 7.5% polyacrylamide
slab gel, pH 8.9, in the absence of denaturants or reducing
agents. Samples were also treated with sodium dodecyl
sulfate (SDS) and dithiothreitol and electrophoresed on a
12.5% polyacrylamide SDS slab gel (for hemoglobin) or
a 4% polyacrylamide SDS slab gel (for hemocyanin) (RYAN
et al., 1985).

The extract of foot tissue was examined spectrophoto-
metrically using a dual beam Gibson spectrophotometer.
The foot tissue extract was also chromatographed on a
calibrated column (1.7 x 24 cm) of Sephadex G-75 su-
perfine in equilibrium with the extraction buffer.

RESULTS

When Leptochiton rugatus was bled, the hemolymph did
not appear red nor did the red color of the animal’s tissues

Page 245

we 200K

oe 116K
—~ s@ 92K

— ——_

Figure 1

SDS PAGE of Leptochiton rugatus hemolymph, 4% polyacryl-
amide. A, Helix aspersa hemocyanin; B, Leptochiton rugatus he-
molymph; C, Katharina tunicata hemocyanin; D, Octopus dofleini
hemocyanin; E, calibrants (myosin, B-galactosidase, phosphory-
lase B).

become lighter. When the foot was removed from the an-
imal, the foot tissue retained its red color.

Examination by SDS gel electrophoresis of the very
small sample of hemolymph obtained from 10 animals
showed no hemoglobin-like subunits. Rather, a strongly
staining protein that electrophoresed to the same position
as the hemocyanin subunit of Katharina tunicata was ob-
served (RYAN ef al., 1985) (Figure 1).

The extract of tissues of foot, gills, and surrounding
mantle shows absorption maxima of 414,540, and 570 nm,
similar to other myoglobins and hemoglobins. The a peak
is shifted slightly to the violet and is lower in absorbance
than the 6 peak; an absorbance ratio of a/B peaks of about
0.85 suggests that the protein is susceptible to oxidation
and that some met-hemoglobin is present. Attempts to
chemically deoxygenate the protein with sodium dithionite
resulted in a typical loss of a and 8 peaks and the ap-
pearance of a smooth peak at about 555 nm. However,
the Soret maximum was shifted to 422-423 nm and not
to 432 nm as seen for other myoglobins and hemoglobins
(LEMBERG & LEGGE, 1949). The most likely interpretation
of these data is that either some of the hemoglobin was
not deoxygenated, some remained in the oxidized met-state
(or as some other derivative) or both.

Chromatography of the sample on a column of Sephadex
G-75 superfine showed a broad peak with a molecular

Page 246

e)
Ww

ABSORBANCE
O
N

g

20 40
ML EFFLUENT
Figure 2

Chromatography of Leptochiton rugatus foot and mantle tissue
extract on Sephadex G-75 superfine. Column buffer, 0.05 M
sodium phosphate, pH 7.5, 0.5 M in NaCl. Calibrants: A, bovine
serum albumen; B, Katharina tunicata dimeric myoglobin; C,
sperm whale myoglobin; D, Katharina tunicata monomeric myo-
globin. Absorbance at 416 nm.

weight slightly less than that of sperm whale myoglobin
(Figure 2) and similar to radular muscle myoglobin of
Katharina tunicata (TERWILLIGER & READ, 1970). Absor-
bance in the void volume was due to turbidity. SDS poly-
acrylamide gel electrophoresis of the foot and mantle tissue
homogenate indicated a strong protein staining band with
a molecular weight of about 15-16,000 (Figure 3D), sim-
ilar to radular myoglobin of K. tunicata under the same
gel conditions (Figure 3B). The radular muscles of Lep-
tochiton rugatus are bright red, with an intensity similar
to the redness of other chiton radular muscles (TERWIL-
LIGER & READ, 1970). A prominent protein band from
the radular muscles of L. rugatus (Figure 3C) migrated to
the same distance upon SDS gel electrophoresis as myoglo-
bins of K. tunicata (Figure 3B). Identification of the 15-
16,000 molecular weight proteins of both foot and radular
tissues as hemoglobin subunits was verified by cross-elec-
trophoresing on SDS the red bands obtained by electro-
phoresis on a pH 8.9 gel in the absence of denaturants
and reducing agents. Owing to very little tissue in both L.
rugatus foot and radular muscle preparations and difficulty
in collecting animals, more detailed studies were not un-
dertaken.

DISCUSSION

Hemoglobins and myoglobins are widespread in mollusks,
where they are found as circulating intra- and extracellular

The Veliger, Vol. 30, No. 3

proteins and in tissues such as buccal muscles, heart, stom-
ach, and nerves (READ, 1966; TERWILLIGER & TERWIL-
LIGER, 1985). There have been no reports of hemoglobin
or myoglobin in the Polyplacophora (chitons) except for
myoglobins found in the bright red buccal musculature,
where both monomeric and dimeric myoglobins are present
(TERWILLIGER & READ, 1970). Furthermore, only he-
mocyanin has been reported as a circulating respiratory
protein in chitons (MANWELL, 1960; VAN HOLDE & MIL-
LER, 1982; RYAN et al., 1985). We find that Leptochiton
rugatus resembles other chitons in having myoglobin in its
radular muscles and having hemocyanin as its circulating
respiratory protein. However, this is the first report of a
more widespread presence of hemoglobin in other tissues
of the chiton. We base our conclusion that the red color is
due to a hemoglobin-like protein on (1) the protein’s ap-
parent molecular weight of 15-16,000 by gel chromatog-
raphy and SDS gel electrophoresis and (2) its hemoglo-
bin-like spectral absorption maxima which change upon
deoxygenation with dithionite. Not enough hemoglobin
was available for O,-binding experiments. Experience with
other tissue hemoglobins, however, suggests that because
the protein is monomeric and not easily deoxygenated with
dithionite, it likely has a high oxygen affinity. We are
referring to this protein as a hemoglobin rather than a
myoglobin because we do not know whether it is found in

Aue BiGaDae
SES Ss YL

68k
43

snr <

Figure 3

SDS PAGE of Leptochiton rugatus hemoglobin-containing tissues,
12.5% polyacrylamide. A, calibrants; B, K. tunicata radular mus-
cle; C, L. rugatus radular muscle; D, L. rugatus foot and mantle
tissue; E, L. rugatus hemolymph. Arrow indicates the position of
tissue hemoglobin.

D. J. Eernisse et al., 1988

muscle fibers in all tissues in which it is present. The
unusual shallow-water habitat for these chitons, under
rocks that are submerged in mud, may point to a reason
for the hemoglobin-rich tissue, in contrast to the presumed
hemoglobin-poor tissue of lepidopleurids that occupy deep
water. The presence of a high-affinity hemoglobin in L.
rugatus might facilitate diffusion of oxygen to respiring
tissues of this organism under hypoxic conditions.

Whatever the connection is between the previously men-
tioned posterior placement and fewer numbers of gill pairs
typical of lepidopleurid chitons and their normal deep-
water habitat, it remains a striking observation that, in
contrast to modern chitons, there are few reported collec-
tions of lepidopleurid chitons from substrates exposed at
low tide. This suggests to us that lepidopleurid chitons
depend on aquatic, rather than aerial, respiration. Yet
Leptochiton rugatus is found in a shallow-water habitat
that appears oxygen poor; in fact, no modern chitons or
other mollusks were observed on the same substrates heavi-
ly populated by L. rugatus. Moreover, at least two other
lepidopleurid species have been reported from similar hab-
itats. IREDALE & HULL (1929) report Terenochiton sub-
tropicalis (=Leptochiton norfolcensis [Hedley & Hull, 1912])
from the Sunday Islands, Kemadec Group (also known
from New Zealand), collected living on the underside of
embedded dirty stones below low water mark. IREDALE &
HULL (1929) also report collecting 60 to 80 specimens of
the Australian species Leptochiton badius (Hedley & Hull,
1909) in one afternoon from under deeply buried stones
between tide marks. A prediction consistent with our hy-
pothesis, that the presence of tissue hemoglobins is related
to the unusual habitat of L. rugatus, would be that the foot
and other tissues of L. subtropicalis and L. badius, like those
of L. rugatus, should be red as well.

ACKNOWLEDGMENTS

This work was supported by NSF grant OCE-8415258
to R. R. Strathmann and D. J. Eernisse and by NSF grant
DMB-8511150 to N. B. Terwilliger and R. C. Terwil-
liger. We thank Dr. A. O. D. Willows for use of facilities
at Friday Harbor Laboratories, University of Washington.

Page 247

LITERATURE CITED

EERNISSE, D. J. 1984. Lepidochitona Gray, 1821 (Mollusca:
Polyplacophora), from the Pacific Coast of the United States:
systematics and reproduction. Ph.D. Thesis, University of
California, Santa Cruz. 358 pp.

EERNISSE, D. J. 1985. The significance of gill placement in
chitons. West. Soc. Malacol. Ann. Rept. 17 (for 1984):8-9
(abstract).

FERREIRA, A. J. 1979. The family Lepidopleuridae (Mollusca:
Polyplacophora) in the eastern Pacific. Veliger 22:145-165.

Hoare, R.D. & A.G. SMITH. 1984. Permian Polyplacophora
(Mollusca) from west Texas. Jour. Paleontol. 58:82-103.

IREDALE, T. & A. F. B. Hutt. 1929. The loricates of the
Neozelanic region (1). Austral. Zool. 6:75-95.

Kaas, P. & R. A. VAN BELLE. 1985. Monograph of living
chitons (Mollusca: Polyplacophora). Vol. 1. Order Neolor-
icata: Lepidopleurina. E. J. Brill/Dr. W. Backhuys: Leiden.
240 pp.

Kaas, P. & R. A. VAN BELLE. 1986. Monograph of living
chitons (Mollusca: Polyplacophora). Vol. 2. Suborder Is-
chnochitonina, Ischnochitonidae: Schizoplacinae, Callochi-
toninae, & Lepidochitoninae. E. J. Brill/Dr. W. Backhuys:
Leiden. 198 pp.

LEMBERG, R. & J. W. LEGGE. 1949. Hematin compounds and
bile pigments. Interscience: New York. 749 pp.

MANWELL, C. 1960. Comparative physiology: blood pigments.
Ann. Rev. Physiol. 22:191-244.

READ, K. R. H. 1966. Molluscan hemoglobin and myoglobin.
Pp. 209-232. In: K. M. Wilbur & C. M. Yonge (eds.),
Physiology of Mollusca. Vol. 2. Academic Press: New York.
645 pp.

Ryan, M., N. B. TERWILLIGER, R. C. TERWILLIGER & E. SCHAB-
TACH. 1985. Chiton hemocyanin structure. Comp. Bio-
chem. Physiol. 80B:647-656.

TERWILLIGER, R. C. & K. R. H. ReaD. 1970. The radular
muscle myoglobins of the amphineuran molluscs, Katharina
tunicata Wood, Cryptochiton steller. Middendorf, and Mopalia
muscosa Gould. Int. Jour. Biochem. 1:281-291.

TERWILLIGER, R. C. & N. B. TERWILLIGER. 1985. Molluscan
hemoglobins. Comp. Biochem. Physiol. 81B:255-261.

VAN BELLE, R. A. 1981. Catalogue of fossil chitons. Dr. W.
Backhuys, Publisher: Rotterdam. 84 pp.

VAN Ho pe, K. E. & K. I. MILLER. 1982. Haemocyanins.
Quart. Rev. Biophys. 15:1-129.

YONGE, C. M. 1939. On the mantle cavity and its contained
organs in the Loricata (Placophora). Quart. Jour. Microsc.
Sci. 81:367-390.

The Veliger 30(3):248-256 (January 4, 1988)

THE VELIGER
© CMS, Inc., 1988

Chromosomes of Some Subantarctic Brooding
Bivalve Species
by

CATHERINE THIRIOT-QUIEVREUX

Universite P. et M. Curie, Station Zoologique, 06230 Villefranche-sur-Mer, France

JACQUES SOYER anp MARC BOUVY

Universite P. et M. Curie, Laboratoire Arago, UA 117, 66650 Banyuls-sur-Mer, France
AND

JOHN A. ALLEN

University Marine Biological Station Millport, Isle of Cumbrae, Scotland KA28 0EG

Abstract. Chromosomes of three subantarctic brooding bivalve species have been studied in relation
to their type of development and the evolutionary distance between their taxonomic categories. Gavmardia
trapesina (Gaimardiidae) has a diploid chromosome number of 2n = 38, with 8 chromosome pairs of
metacentrics, 7 pairs of submetacentrics, and 4 pairs of subtelocentrics. Kidderia bisulcata (Cyamiidae)
has 2n = 38, with 3 pairs of metacentrics, 4 pairs of submetacentrics, 7 pairs of subtelocentrics, and 5
pairs of telocentrics. Kidderia minuta, another species of Cyamiidae, has 2n = 36, with 3 pairs of
metacentrics, 2 pairs of submetacentrics, 8 pairs of subtelocentrics, and 5 pairs of telocentrics. The
karyological features of these species are not related to direct development and the brooding of the
developing eggs. Evolutionary considerations based on comparison of the chromosomes of the families
investigated (the Gaimardiidae and the Cyamiidae) suggest that they are phylogenetically primitive.
The recent transfer of Kidderia bisulcata (=Hiatella bisulcata) from the Hiatellidae (Myoida) to the
Cyamiidae (Veneroida) is questioned, and further morphological study is required to determine its true
taxonomic position. It is also clear that the evolutionary pattern of karyological features remains

unsatisfactory without further investigations of eulamellibranch species.

INTRODUCTION

Cytogenetic studies of chromosome number and morphol-
ogy might not only show genetic variation between species
and populations, but also evolutionary relationships within
different taxonomic groups. The knowledge of the chro-
mosomes in the Bivalvia has increased over the last 15
years. NAKAMURA (1985) reviewed recent investigations
on chromosomes of 125 bivalve species belonging to 22 of
the 102 Recent families. Of these 125 species, 73 belong
to the Mytilidae, Pectinidae, Ostreidae, and Unionacea;
the other species are scattered mostly within the Pterio-
morpha, with fewer within the Heterodonta. Thus, evo-
lutionary interpretation of karyological characteristics re-

mains hazardous without further investigations, especially
as the chromosomes of the primitive groups of bivalves
have rarely been investigated. Exceptions are two species
of Solemyidae (IEYAMA, 1982) and seven species of Arcidae
(IEYAMA, 1975, 1983, 1984a, b). A further point of interest
concerning primitive bivalves is that non-planktotrophic
development appears to be the rule for primitive groups,
such as the Protobranchia, Septibranchia, and the eula-
mellibranch superfamilies Lucinacea and Crassatellacea
(JABLONSKI & LuTZz, 1983). Most other bivalve species
have planktotrophic development.

Non-planktotrophic development combined with brood
protection constitutes a specialized type of development
that occurs among some primitive superfamilies (Arcacea,

C. Thiriot-Quievreux ef al., 1988

Leptonacea, and Cyamiacea). Antarctic Bivalvia have a
relatively large percentage of species within these super-
families (DELL, 1972; ARNAUD, 1974; RICHARDSON, 1979).

In a research program on the evolutionary genetics of
benthic species from the subantarctic Kerguelen Islands,
we selected four species (with direct development and
brooding of young) in order to study their chromosomes
and to appreciate whether their karyological features may
reflect a development type or a phylogenetic trend.

The present paper gives karyological data on three of
these species, namely: Garmardia trapesina (Lamarck, 1819)
(Heterodonta, Veneroida, Gaimardiacea, Gaimardiidae);
Kidderia bisulcata (Smith, 1879); and Kidderia minuta (Dall,
1876) (Heterodonta, Veneroida, Cyamiacea, Cyamiidae).
Because of their peculiar characteristics, the chromosomes
of the fourth species investigated, Lasaea consanguinea
(Smith, 1877) (Heterodonta, Veneroida, Leptonacea, La-
saeidae), are to be described in a separate paper.

Classification follows NEWELL, 1969 (see also, OLD-
FIELD, 1964; PONDER, 1967; SIMPSON, 1977; MORTON,
1979; RICHARDSON, 1979; Boss, 1982; O’FOIGHIL, 1986).
Detailed comparisons have been made with Antarctic ma-
terial housed in the British Museum (Natural History).

MATERIALS anD METHODS
Sampling

Populations of Kidderia minuta were collected by hand
at low tide in the intertidal zone under rocks in a well
sheltered area ““Halage des Swains,” in the southwest part
of the Gulf of Morbihan, Kerguelen Islands.

Specimens of Kidderia bisulcata and Gaimardia trapesina
were collected among algae in minute pools of a small reef,
exposed only at low tide at Ratmanoff, on the east coast
of the Kerguelen Islands.

Chromosome Preparations

Whole animals were treated 2-4 h with 0.005% col-
chicine in seawater. Then the bodies were removed from
their shells under the dissecting microscope and treated 40
min in 0.9% sodium citrate. The material was then fixed
in a freshly prepared mixture of absolute alcohol and acetic
acid (3:1) with three changes of 20 min duration. Each
slide preparation was made from three to five bodies fol-
lowing an air-drying technique (THIRIOT-QUIEVREUX &
AYRAUD, 1982). The preparations were stained with
Giemsa (4%, pH 6.8) and photographs of suitable meta-
phases were taken with a Zeiss II photomicroscope. Cell
divisions were mainly observed in gonadic tissue.

Data Analysis

The number of chromosomes seen in the photomicro-
graphs of at least 30 spread metaphases were counted for
each species. Then the photographs of individual chro-

Page 249

mosomes from the better spreads were cut out and arranged
in pairs on the basis of size and centromere position for
the karyotypes.

Measurements of chromosomes were made with a dig-
itizer (Bit Pad 10, Summa graphic), interfaced with a
Victor S1 microcomputer (THIRIOT-QUIEVREUX, 1984).
Relative length or percent total complement length was
expressed as 100 times the absolute chromosome pair length
divided by the total length of the haploid complement.
Centromeric indexes (Ci) were calculated by dividing 100
times the length of the short arm by the total chromosome
length. Terminology relating to centromeric position fol-
lows that of Levan et al. (1964). A chromosome is meta-
centric (m) if Ci falls in the range 37.5-50.0, submeta-
centric (sm) if Ci is 25.0-37.5, subtelocentric (st) if Ci is
12.5-25.0, and telocentric (t) if Ci is 0.0-12.5. When a
centromere position was found to be on the borderline
between two different categories the confidene limit of the
means was calculated as P = 0.05 and two chromosome
categories are listed. The arm ratio is calculated as length
of short arm divided by the length of the long arm. The
centromeric index and the arm ratio are given, as both
express centromeric position and allow comparison with
previous studies.

RESULTS
Gaimardia trapesina

The chromosomes of 31 mitotic metaphase spreads were
counted. Seventeen cells showed 2n = 38, 14 cells had an
aneuploid number of 33 to 37. A haploid number of 19
was counted in three meiotic metaphases. Thus the diploid
chromosome number for this species is 2n = 38.

Means and standard deviations of relative length, arm
ratio, and centromeric index for seven well-spread meta-
phases from different animals are given in Table 1.

From data on relative length, we recognize five groups
of chromosome pairs of decreasing size and, from the cen-
tromeric index, we characterize the morphological type of
each chromosome pair. Thus, the karyotype (Figure 1) of
Gaimardia trapesina consists of:

Group I: pair 1 metacentric, obviously larger than the
remainder.

Group II: pairs 2, 3, 4, 5, 7 submetacentric; pair 6
subtelocentric.

Group III: pairs 8 and 9 submetacentric; pair 10 sub-
telocentric to submetacentric, pair 11 subtelocentric.

Group IV: pairs 12 to 15 metacentric.

Group V: pairs 16 to 18 metacentric and pair 19 sub-
telocentric.

In order to visualize better the different types of chro-
mosome pairs, we have constructed an ideogram from cen-
tromeric indexes and relative length values. The ideogram
for Gaimardia trapesina (Figure 2) shows a conspicuous

Page 250 The Veliger, Vol. 30, No. 3
Table 1
Chromosome measurements and classification in seven cells for Gazmardia trapesina.
Chromo- ; : fan
5 Relative length Arm ratio Centromeric index ;
SOOTVUG™ pau ea re eee ere aSsitica=
Group number Mean SD Mean SD Mean SD tion

I 1 11.92 0.914 0.811 0.058 44.61 1.858 m
II 2 6.69 0.307 0.464 0.043 31.53 1.979 sm
II 3 6.23 0.308 0.413 0.054 29.00 2.800 sm
II 4 6.11 0.258 0.448 0.043 30.66 DAS sm
II 5 5.87 0.269 0.490 0.051 32018 2.379 sm
II 6 5.61 0.523 0.306 0.059 23.19 3.567 st
II i Do) 0.494 0.428 0.120 28.43 4.166 sm
Ill 8 5.21 0.438 0.506 0.050 33.34 2.264 sm
III 9 5.11 0.501 0.478 0.051 32.11 2.357 sm
Ill 10 5.06 0.614 0.335 0.088 24.70 4.834 st-sm
III 11 4.75 0.726 0.296 0.061 DSi 3.577 st
IV 12 4.49 0.433 0.810 0.115 44.38 3.569 m
IV 13 4.33 0.279 0.873 0.077 46.23 2.131 m
IV 14 4.19 0.383 0.848 0.150 45.40 4.219 m
IV 15 4.11 0.541 0.819 0.173 44.28 6.271 m
Vv 16 3.91 0.304 0.937 0.698 48.08 1.794 m
Vv 17 3.80 0.223 0.893 0.158 46.44 4.536 m
Vv 18 3.66 0.318 0.861 0.061 45.90 1.745 m
Vv 19 3.37 0.456 0.295 0.110 22.14 6.862 st

disparity of size between the pair 1 and the other pairs.
Three different types of chromosomes are present: meta-
centric, submetacentric, and subtelocentric.

We summarize karyological data for this species with
the formula: 2n = 38 = 8m, 7sm, 4st = 15m-sm/4st.

nk
Bh AK KA
58 3x A464

9 10

Rs 33 aw
12 13

Kidderia bisulcata

The chromosome of 35 mitotic metaphases were count-
ed. Twenty-eight cells had 2n = 38, 7 cells had 2n = 36
or 37. Meiotic metaphases were abundant and we scored
36 cells, of which 32 showed a haploid number of 19 and

Ra 5 ym

14 15
RB Be ean en
16 17 18 19
Figure 1

Karyotype of Gaimardia trapesina.

C. Thiriot-Quievreux ef al., 1988

Relative length

Figure 2

Chromosome pair

Ideogram of the different types of chromosomes for Gazmardia trapesina.

Table 2

Chromosome measurements and classification in eight cells for Kzdderia bisulcata.

12

10

5

Claveine Relative length
some pair

Group number Mean SD
I 1 8.24 1.075
I 2 V2 0.535
I 3 6.65 0.272
II 4 6.39 0.522
II 5 6.38 0.437
II 6 6.05 0.370
II 7 5.69 0.534
II 8 5.66 0.282
Ill 9 5.36 0.155
III 10 5335) 0.469
Ill 11 5232 0.356
Ill 12 4.99 0.343
Ill 13 4.95 0.323
IV 14 4.13 0.593
IV 15 3.91 0.350
IV 16 3.85 0.449
IV 17 3.54 0.564
IV 18 3.35 0.470
Vv 19 2.86 0.324

Mean

0.685
0.102
0.425
0.107
0.309
0.288
0.129
0.213
0.127
0.139
0.695
0.435
0.343
0.180
0.199
0.455
0.196
0.203
0.709

Arm ratio
SD

0.180
0.015
0.163
0.034
0.107
0.118
0.028
0.172
0.027
0.028
0.105
0.076
0.081
0.041
0.083
0.092
0.055
0.045
0.180

Centromeric index

Mean

39.76

9.24
28.49

9.55
23.01
21.78
11.40
15.71
LES
12.11
39.68
29.76
25.03
15.09
16.01
30.80
16.10
16.56
40.51

SD

6.603
1.294
6.714
2.783
5.987
6.193
2.216
6.901
2.114
2.138
5.743
3.106
4.591
2.968
4.778
4.600
Sol 1a)
2.944
6.382

Page 251

Classifica-
tion

Page 252

The Veliger, Vol. 30, No. 3

fe |g
v os
1 2
>. 9 72
* , 4 4
} ,, 3, ‘ “ * ‘ \" ’
4 5 7 8
4
EX ff 3} Bh Gp
9 10 12 13
Ag &* “ “ee
4 ? 5A . ") ,
14 15 17 18
Ox 5 ym
19
Figure 3

Karyotype of Kidderia bisulcata.

2 with 18. Thus, the diploid chromosome number for this
species is 2n = 38.

For karyotyping, eight well-spread metaphases from
different animals were analyzed (Table 2). The karyotype
(Figure 3) of Kidderia bisulcata consists of five groups of
chromosome pairs with a regular decrease in size:

Group I: pair 1 metacentric, pair 2 telocentric, pair 3
submetacentric.

Group II: pairs 4-8 subtelocentric or telocentric. The
pairs 4 and 5, 7 and 8 are very close in relative length
and it is difficult to identify them with rigor; however,
the position of the centromere is always telocentric in
pair 4 and telocentric to subtelocentric in pair 7.

Group III: pairs 9 and 10 are very similar, telocentric
to subtelocentric, pair 11 metacentric, pair 12 sub-
metacentric, pair 13 submetacentric-subtelocentric.
The last two pairs are also very similar and can be
confused.

Group IV: pairs 14 and 15 subtelocentric, pair 16 sub-
metacentric, pairs 17 and 18 subtelocentric.

Group V: pair 19 metacentric and obviously the smallest.

The ideogram (Figure 4) shows the distribution of the
four chromosome types. We summarize karyological data

for this species with the formula: 2n = 38 = 3m, 4sm, 7st,
5t = 7m-sm/12st-t.

Kidderia minuta

The chromosomes of 36 mitotic metaphases were count-
ed. Twenty-nine cells had 2n = 36, 7 cells had an aneuploid
diploid number varying from 32 to 36. Ten meiotic me-
taphases were also counted, 9 with n = 18, 1 withn = 19.
The diploid chromosome number for this species is 2n =
36.

The chromosome measurements and classification were
analyzed for seven examples of well-spread metaphases,
each from a different animal (Table 3).

The karyotype (Figure 5) consists of six groups of chro-
mosome pairs of decreasing size, the first group being much
larger than the other groups, for the latter rank order of
decreasing size is relatively regular:

Group I: pair 1 metacentric.

Group II: pair 2 telocentric, pair 3 metacentric, pairs 4
and 5 telocentric.

Group III: pair 6 submetacentric-subtelocentric, pair 7
telocentric, pair 8 metacentric, pair 9 telocentric.

Group IV: pairs 10 to 12 subtelocentric.

C. Thiriot-Quievreux ef al., 1988

Relative length

Page 253

m sm

st t

Chromosome pair

Figure 4

Ideogram of the different types of chromosomes for Kidderia bisulcata.

Group V: pairs 13 to 15 subtelocentric.
Group VI: pairs 16 and 17 subtelocentric, pair 18 sub-
metacentric—metacentric.

The ideogram (Figure 6) clearly shows the disparity of
size between pair 1 and the other pairs. Four morpholog-
ical types of chromosomes are present but subtelocentric
and telocentric types are dominant in this species.

We summarize karyological data for this species with
the formula: 2n = 36 = 3m, 2sm, 8st, 5t = 5m-sm/13st-t.

DISCUSSION

There is considerable debate in the literature as to the
exact relationships of the Gaimardiacea and the Cyami-
acea (MorTON, 1979). Until recently, both superfamilies
were included in the Veneroidea although widely separated
in the classification of the order (NEWELL, 1969). MORTON
(1979) in his study on Neogaimardia finlay: questioned this
and concluded that the gaimardiids were closely related to
the cyamiids, however, admitting that more comprehensive
studies were necessary to be certain. PONDER (1971) in-
cluded the Gaimardiinae as a subfamily in the Cyamiacea.
Furthermore, Boss (1982) transferred the genus Kidderia
from the subfamily Gaimardiinae to the family Cyamiidae
and, following PONDER (1971), he reinstated the Gaimar-
diidae to family rank.

The problem is further complicated by the fact that
Kidderia bisulcata was originally described as a species of
Saxicava (=Hniatella) by SMITH (1879). It was still regarded

as such by POWELL (1957) but later considered to be a
species of Kidderia by DELL (1969). The shell features,
including radial grooves, elongate opisthodetic ligament,
and hinge structure, would lead one to conclude that it is
a hiatellacean species. In contrast, K. minuta has no radial
grooves and a much thinner hinge plate with cardinal teeth
of a different form, although the opisthodetic ligament
(more internal in position) is massive and elongate.

Although detailed morphological comparisons need to
be carried out, comparison of the karyological data of these
three brooding bivalve species does not show close rela-
tionship. Moreover, a fourth brooding species investigated,
Lasaea consanguinea, is totally different, in showing an
unusually high number of chromosomes (THIRIOT-
QUIEVREUX ef al., in press).

Karyological features are generally species specific and
consequently could be related to the evolutionary distance
between taxonomic categories. Chromosome data for ve-
neroid bivalves are only recorded for more recent families,
such as the Cardiidae, Mactridae, Donacidae, Corbiculi-
dae, Pisididae, and Veneridae (NAKAMURA, 1985) and the
diploid chromosome complement is 2n = 36 or 2n = 38
(except for the Pisididae). Three species of Veneridae have
been karyologically investigated and show 2n = 38 = 19m-—
sm (IEYAMA, 1980). We have found the same karyological
data for Ruditapes philippinarum, another venerid species
(personal observations). Nevertheless, within the Cardi-
idae, a family with a more primitive phylogenetic position,
one species, Cerastoderma edule, shows karyological data

Page 254

The Veliger, Vol. 30, No. 3

Table 3

Chromosome measurements and classification in seven cells for Kidderia minuta.

Chiro Relative length Arm ratio Centromeric index ;
some pair Classifica-
Group number Mean SD Mean SD Mean SD tion
I 1 14.64 0.836 0.783 0.070 43.55 2.393 m
II 2 8.04 0.734 0.094 0.022 8.57 1.842 t
Il 3 6.87 0.697 0.851 0.108 45.73 3.134 m
II 4 6.75 0.709 0.102 0.024 9.18 2.059 t
Il 5 6.17 0.577 0.106 0.014 9.57 1.168 t
III 6 557/5) 0.599 0.374 0.075 26.89 3.999 sm-st
Il q 5.61 0.367 0.123 0.019 10.91 1.541 t
Ill 8 5.38 0.591 0.751 0.148 42.31 4.657 m
Ill 9 5.24 0.348 0.124 0.028 10.89 2.215 t
IV 10 4.68 0.366 0.311 0.122 21.84 5.232 st
IV 11 4.57 0.211 0.155 0.045 13.31 3.176 st
IV 12 4.49 0.245 0.154 0.022 13.23 1.627 st
Vv 13 4.24 0.227 0.173 0.043 14.60 3.160 st
V 14 3.98 0.201 0.153 0.022 13.23 1.732 st
Vv 15 3.86 0.332 0.327 0.130 22.68 5.947 st
VI 16 3.39 0.441 0.166 0.046 14.01 3.476 st
VI 17 3.28 0.308 0.186 0.050 15.41 3.542 st
VI 18 2.99 0.415 0.643 0.336 36.40 14.695 sm-m
of 2n = 38 = 7sm/12st-t (KOULMAN & WOLFF, 1977).
The two species of the family Cyamiidae studied here,
Kidderia bisulcata with 2n = 38 = 7m-sm/12st-t and K.
\ minuta with 2n = 36 = 5m-sm/13st-t are karyologically
closer to the Cardiidae than to the Veneridae so far in-
vestigated. As reported above there is some doubt as to
whether K. bisulcata is a cyamiid, but both species are
1 characterized by a variable diploid complement and the
presence of the four chromosomal types, the majority being
st-t.
> f f | Ah A a A variable number of chromosomes combined with the
' presence of st-t chromosomes reflects variable karyotypes
2 3 4 5 (WHITE, 1973). In contrast, a majority of m-sm chro-
mosomes suggests a stable karyotype (NAKAMURA, 1985).
& “ 4 | rad * | Thus, the karyotypes of two species of Cyamiidae and one
a x : species of Cardiidae seem less stable than those of kary-
6 7 8 9 ologically known species of the family Veneridae. Gai-
mardia trapesina, with a majority of metacentrics, sub-
a “a & *® a metacentrics, and a few subtelocentrics, could tentatively
§ be considered to show a more stable karyotype and there-
10 11 12 fore have an intermediate position between the Cyamiidae
and the Veneridae. But without further investigation of
a & A & 4 A Sym other species of the Veneroida, the evolutionary pattern of
karyological features remains incomplete and unsatisfac-
13 14 15 tory.
All the evidence points to the fact that the three species
% A & -» eo studied here are phylogenetically separated and supports
16 17 18 the earlier determinations that the Cyamiacea and Gai-
: mardiacea are distinct from each other. So-called Kidderia
Figure 5 bisulcata may indeed be a species of Hiatella (=Saxicava).

Karyotype of Kidderia minuta.

The issue is made more complex by convergence of form

C. Thiriot-Quievreux ez al., 1988

length

Relative
14

10

Page 255

m sm st

t

Figure 6

Ideogram of the different types of chromosomes for Kidderia minuta.

and reproduction in bivalves of southern high latitudes,
which will be the object of further studies.

ACKNOWLEDGMENTS

This work is part of a research program on the evolu-
tionary genetics of benthic species from the Kerguelen
region sponsored by the T.A.A.F. (Terres Australes et
Antarctiques Frangaises). We are especially grateful to the
staff of the “Mission de la Recherche,” T.A.A.F. for as-
sistance in obtaining specimens in the field at Kerguelen.
Wealso thank P. Albert and G. Quelard for their excellent
technical assistance.

LITERATURE CITED

ARNAUD, P. M. 1974. Contribution a la bionomie benthique
des régions antarctiques et subantarctiques. Tethys 6:465-
653.

Boss, R. T. 1982. Mollusca. Pp. 945-1166. In: S. Q. Parker
(ed.), Synopsis and organization of living organisms.
McGraw-Hill: New York.

DELL, R. K. 1969. Antarctic and subantarctic Mollusca: Am-
phineura, Scaphopoda and Bivalvia. Disc. Rept. 33:93-250.

DELL, R. K. 1972. Antarctic benthos. Adv. Mar. Biol. 10:1-
216.

IEYAMA, H. 1975. Chromosome numbers of three species in
three families of Pteriomorphia (Bivalvia). Venus 34:26-32.

IEYAMA, H. 1980. Studies on the chromosomes in three species
of the Veneridae (Bivalvia). Venus 39:49-55.

IEYAMA, H. 1982. Karyotypes in two species of the Solemyidae
(Bivalvia, Cryptodonta). Venus 40:232-236.

IEYAMA, H. 1983. Somatic chromosomes of the arcid Arca bou-
cardi (Bivalvia, Pteriomorphia). Chromosome Inf. Serv. 35:
3-4,

IEYAMA, H. 1984a. Chromosomes of six species in three families
of Pteriomorphia (Bivalvia). Venus 43:106-111.

IEYAMA, H. 1984b. Chromosome numbers in three species of
bivalves (Pteriomorpha: Mollusca). Chromosome Inf. Serv.
36:15-16.

JABLONSKI, D. & R. A. Lutz. 1983. Larval ecology of marine
invertebrates: paleobiological implications. Biol. Rev. 58:21-
89.

KouLMan, J. G. & W. S. WoutrFr. 1977. The Mollusca of the
estuarine region of the rivers Rhin, Meuse and Scheldt in
relation to the hydrography of the area. V. The Cardidae.
Basteria 41:21-32.

Page 256

LEVAN, A., K. FREDGA & A. A. SANDBERG. 1964. Nomencla-
ture for centromere position in chromosomes. Hereditas 52:
101-220.

Morton, B. 1979. The biology, functional morphology and
taxonomic status of Gazmardia (Neogaimardia) finlay (Bi-
valvia Gaimardiidae). Jour. Zool. 188:123-142.

NAKAMURA, H. K. 1985. A review of molluscan cytogenetic
information based on the CISMOCH-computerized system
for molluscan chromosomes. Bivalvia, Polyplacophora and
Cephalopoda. Venus 44:193-225.

NEWELL, N. D. 1969. Outline of classification. Pp. 218-224.
In: R. C. Moore (ed.), Treatise on invertebrate palaeontol-
ogy, Part N 1: Mollusca 6. Bivalvia. Univ. Kansas Press:
Lawrence.

O’FoIGHIL, D. 1986. Prodissoconch morphology is environ-
mentally modified in the brooding bivalve Lasaea subviridis.
Mar. Biol. 92:517-524.

OLDFIELD, E. 1964. The reproduction and development of some
members of the Erycinidae and Montacutidae (Mollusca,
Eulamellibranchia). Proc. Malacol. Soc. Lond. 36:79-120.

PONDER, W. F. 1967. Observations on the living animals and
mode of life of some New Zealand erynacean bivalves. Trans.
Roy. Soc. N.Z. Zool. 10:21-32.

PONDER, W. F. 1971. Some New Zealand and subantarctic
bivalves of the Cyamiacea and Leptonacea with descriptions
of new taxa. Rec. Dom. Mus. Wellington 7:119-141.

The Veliger, Vol. 30, No. 3

POWELL, A. W. B. 1957. Antarctic and subantarctic Mollusca.
Rec. Auckland Inst. Mus. 5:117-193.

RICHARDSON, M. G. 1979. The ecology and reproduction of
the brooding Antarctic bivalve Lissarca miliaris. Brit. Ant.
Surv. Bull. 44:125-142.

SIMPSON, R. D. 1977. The reproduction of some littoral mol-
lusecs from Macquaries Island (sub-Antarctic). Mar. Biol.
44:125-142.

SMITH, E. A. 1879. An account of petrological, botanical and
zoological collections made in Kerguelen’s land and Rodri-
guez during the years 1874-75. Phil. Trans. Roy. Soc. Lond.
168:167-192.

THIRIOT-QUIEVREUX, C. 1984. Chromosome analysis of three
species of Mytilus (Bivalvia: Mytilidae). Mar. Biol. Lett. 5:
265-273.

THIRIOT-QUIEVREUX, C. & N. AYRAUD. 1982. Les caryotypes
de quelques espéces de bivalves et de gasteropodes marins.
Mar. Biol. 70:165-172.

THIRIOT-QUIEVREUX, C., J. SOYER, F. DE BOVEE & P. ALBERT.
In press. Unusual chromosome complement in the brooding
bivalve Lasaea consanguinea. Genetica.

WuiteE, H.S. D. 1973. Animal cytology and evolution. 3rd ed.
Cambridge University Press. 961 pp.

The Veliger 30(3):257-266 (January 4, 1988)

THE VELIGER
© CMS, Inc., 1988

Reproduction and Growth of the Brooding

Bivalve Transennella tantilla

MARY ANN ASSON-BATRES!

University of Oregon, Institute of Marine Biology,
Charleston, Oregon 97420, U.S.A.

Abstract.

Transennella tantilla from the South Slough of Coos Bay, Oregon, grow and reproduce

year-around. Fecundity and release of young are seasonally variable. Males are smaller than females,
and the transition from male to female is progressive over a broad size range, supporting histologic
studies that indicate the species is protandric. Mortality is primarily focused on the largest size classes
(>2.0 mm, shell length) and appears to be caused by intense seasonal predation. Individuals of T. tantilla
are larger and appear to be more abundant in False Bay on San Juan Island, Washington, than in the
South Slough of Coos Bay. Because these differences are so striking, several life-history traits of animals
from the two areas were compared. In False Bay, males reach larger sizes and females begin brooding
when larger; egg size is similar, but False Bay females have smaller broods and release young at a
larger size than females in South Slough. The fecundity of female 7. tantilla from both geographic

locations is a linear function of body size.

INTRODUCTION

The venerid bivalve 7ransennella tantilla (Gould, 1852)
inhabits intertidal soft-substrate communities from Alaska
to Lower California (KEEN, 1937). Its maximal size varies
with geographic location; the reported range is 5.30-7.00
mm in shell length (Gray, 1978; AssON-BATRES, 1982).
It has been described as a protandrous hermaphrodite
(HANSEN, 1953). It is ovoviviparous, and mature females
are found with broods of embryos and young in all stages
of development during every season.

The associations of (1) small size and brooding and (2)
small size and protandry have been observed so often that
they have prompted investigators to suggest these pairs of
traits may be coadapted (SELLMER, 1967; MENGE, 1975;
CHRISTIANSEN & FENCHEL, 1979; CHARNOV, 1982). Be-
cause of its life-history traits (small size relative to other
venerids, brooding behavior, and protandry), Transennella
tantilla is an appropriate model for tests of coadaptation.

The purpose of this study was to provide a detailed
description of the reproductive traits of Transennella tan-
tilla from the South Slough of Coos Bay in Oregon. Fe-
cundity was also monitored in females collected from False

"Current address: Oregon Health Sciences University, Heart
Research Lab L464, 3181 S.W. Sam Jackson Park Road, Port-
land, Oregon 97201, U.S.A.

Bay on San Juan Island, Washington, where the species
grows larger and appears to be more numerous. A com-
parison of latitudinal differences in the reproductive be-
havior of 7. tantilla was of interest because differences in
the size of females, brood size, or juvenile release size at
the two locations could be important determinants of the
increased size and apparent abundance of 7. tantilla at
False Bay.

SAMPLING DESIGN

Data collections were designed to obtain information on
protandry, fecundity, egg size, juvenile release size, sea-
sonality of reproduction and growth, and size frequencies
of Transennella tantilla in the South Slough of Coos Bay,
Oregon. The purpose of the sampling protocol was to
obtain representative data to describe these life-history
parameters; it was not intended to provide data on absolute
population densities within given areas.

The distribution of Transennella tantilla within the com-
munity is patchy (OBREBSKI, 1968). In Coos Bay, adults
and juveniles occupy the upper 1-2 cm of sediment and
are generally not evident until one perturbs the sediment
surface. The clam secretes a byssal thread that anchors it
to the grains of sediment, offering some resistence to dis-
persal by wave action (NARCHI, 1970). In areas of strong
wave action (boat swells around the base of piers) or in

Page 258

The Veliger, Vol. 30, No. 3

PACIFIC
OCEAN

COOs

Bay

5O°N

46°N

42°N

Figure 1

Map of the South Slough of Coos Bay, Oregon, indicating the
location of the five study sites: PA, PB, PC, MP, and MS. Offset
indicates the geographic location of Coos Bay (CB), Oregon, and
False Bay (FB) on San Juan Island, Washington.

areas of fast water runoff during low tide, the clams (par-
ticularly those in the largest size classes) are swept along
and deposited on the slopes of troughs sculptured by the
current. In Coos Bay, the clams are subject to (1) anoxia
and (2) burial by shifting sediments during seasonal storms
and dredging operations.

The sampling strategy that was adopted for this study
took into consideration the distribution of Transennella
tantilla in the mudflat community and the potential for
environmental factors to disrupt established populations.
Time was a consideration because sieves that retain 7.
tantilla also retain a considerable amount of sediment which
must be microscopically examined for removal of clams.

Size frequencies and protandry were monitored at Coos
Bay by collecting a single monthly sample at each of five
separated sites on the South Slough mudflat (see Study
Sites section below). Given the patchy distribution of T7an-
sennella tantilla and the potential for a catastrophe (such
as storm waves, sediment deposition, or human activity)
to wipe out the population at a particular site, it was
preferable to regard the mudflat as a single large site and
to collect samples at five discrete locations. To allow tests
of within sample disparity at each mudflat location, each
sample was divided into three equal subsamples in the
field, and each subsample was collected and analyzed sep-
arately.

A caging experiment was designed to provide qualita-

tive, rather than quantitative, information on the time of
growth and release of juvenile 77vansennella tantilla at Coos
Bay.

For geographic comparison of female fecundity, samples
of Transennella tantilla were periodically hand collected
from Coos Bay and False Bay. Details and schedules spe-
cific to this sampling procedure and those discussed above
are described in the Materials and Methods section below.

SOD YS SES

Field studies were conducted at five defined sites (PA, PB,
PC, MP, and MS) on the South Slough mudflat of Coos
Bay, Oregon (43.8°N). The South Slough empties into the
main channel of Coos Bay, approximately 1.3 km from
the mouth of the bay (Figure 1). The sites were picked
because they were representative of areas where T7vansen-
nella tantilla is commonly found on the South Slough mud-
flat. All sites were accessible on most low tides and were
relatively free of human disturbance. The tidal heights
were similar at each location: +0.58 m, +0.34 m, +0.73
m, +0.76 m, and +1.13 m above mean lower low water
at sites PA, PB, PC, MP, and MS respectively.
Transennella tantilla was also collected bimonthly at False
Bay on San Juan Island, Washington (48.5°N, Figure 1).

MATERIALS anD METHODS

Monthly samples were collected from each of the five sites
on the South Slough mudflat from February to December
1981. Transennella confusa also occurs in the South Slough
of Coos Bay (GRay, 1982), but only 7. tantilla was used
in this study. Each month, the sites were searched to de-
termine if major changes in clam densities had occurred.
Areas where obvious changes were noted (7.e., areas that
were anoxic, traversed by streams, or where clams were
absent) were excluded, and a sample was selected by ran-
domly tossing a circular sampler (diameter = 35.7 cm,
area = 0.1 m?) onto the substrate in another area within
the site. Sediment to a depth of 4 cm was removed from
each subsample and sieved with a 500-um mesh screen.
This mesh size was chosen because it retained animals
greater than or equal to 800 wm in shell length and an
amount of sediment that could be microscopically sorted
in a reasonable amount of time. Sieved subsamples were
preserved in 70% isopropyl alcohol.

Shell lengths of all clams in the preserved subsamples
were measured with an ocular micrometer and the results
were grouped into 16 size classes by site and by month. A
total of 2099 Transennella tantilla were removed from the
subsamples collected at sites PA, PB, MP, and MS during
the months of March, April, May, July, August, October,
and December, and were dissected to determine the size
range of males and females. When brooded embryos were
not present, sex was determined by examining gonads.
Testes in preserved specimens were white, translucent,
branching structures; ovaries were globular and contained
white or light yellow eggs that were irregular in shape.

M. A. Asson-Batres, 1988

Page 259

Because of the difficulty of dissecting smaller specimens,
only individuals greater than or equal to 1.85 mm in shell
length were sexed. It was possible to identify the sex of
over 98% of the clams examined. The other 2% were either
sexually undeveloped or were infected with gonad parasites
that obscured identification. Questionable specimens were
not included in the sex ratio analysis. Clams from samples
collected at site PC were not sexed because fewer than 25
animals were 1.85 mm or longer in the entire 0.1-m?
sample (data for all subsamples combined) for five of the
seven months considered.

To assess directly the time of growth and release of
offspring in Coos Bay, Transennella tantilla individuals
were retained in the field in cages made of plastic tubes,
3.0 cm in diameter < 4.0 cm in height, with fabric affixed
to each end (approximate mesh size = 0.35 mm, the height
of newly released juveniles). A detailed description of cage
construction is available in ASSON-BATRES (1982). Each
cage was half-filled with supratidal bay sand, and one
measured clam, 1.0-4.4 mm in shell length, was added.
The cages were brought to the laboratory for examination
on a monthly or bimonthly schedule. They were held for
less than 24 h in outdoor, running seawater aquaria before
and after examination. The lengths of all survivors were
recorded. Because time was a factor and females cannot
be identified externally, only the sediment in cages with
survivors greater than 2.67 mm in shell length was mi-
croscopically examined for the presence of offspring. Sur-
vivors (with the exception of offspring) were returned to
their cages with fresh sand and dead clams were replaced.
Eight trays of 28 cages each were followed on the South
Slough mudflat from December 1980 to June 1981; five
trays of 28 cages each were followed from June to De-
cember 1981.

To determine female size at maturity, brood size, and
the relationship between fecundity and female size or sea-
son, specimens of 7vansennella tantilla were collected by
hand from the South Slough mudflat in July 1980 and
monthly from October 1980 to December 1981. The or-
ganisms were retained at 4°C in glass culture dishes filled
with fresh seawater. Female lengths were measured, and
embryos were removed from the gills and counted. Egg
diameters and embryo lengths were measured to the near-
est 0.01 mm under 200 magnification. Whole animal
(shell included) weights of 7. tantilla collected during Oc-
tober, November, and December 1980 were determined.
Wet weights were recorded to the nearest 0.1 mg.

Samples of Transennella tantilla were hand collected from
False Bay in May 1980, and bimonthly from November
1980 to October 1981. Living clams were retained and
analyzed as described above.

RESULTS
Subsample Analysis
A single classification analysis of variance with repeated

measures (PHILLIPS, 1978) was carried out to compare
subsample densities. Data from each site were analyzed

Table 1

Sex structure of the 7ransennella tantilla population at sites
PA, PB, MP, and MS on the South Slough of Coos Bay,
Oregon, sampled from March to December 1981.

Size class
(mm)* nt % male
1.85-2.07 758 89
2.15-2.37 592 70
2.44-2.66 326 36
2.74-2.96 187 12
>2.96 236 1

* Shell lengths were measured in divisions with an ocular mi-
crometer. Conversion of divisions into mm (100, one division =
0.074 mm) results in discontinuous size-class groupings.

+ n indicates the number of animals examined.

independently. For a given month, at a given site, subsam-
ple densities were always comparable (P > 0.60). As a
result, subsample data were combined for further analyses.

Size Range of Males and Females

The wet tissue weight (WTW, mg) of Transennella
tantiulla was related to shell length (SL, mm) by the regres-
sion, logy,WTW = 3.04 logiSL — 0.54 (SD,g, = 0.06;
r? = 0.98; n = 42). Because there was a good correlation,
the anteroposterior dimension (length) was used as an
indicator of clam weight.

Shell lengths of Transennella tantilla ranged from 0.55
to 5.33 mm. The largest male found during the study was
3.48 mm (dissected live, January 1981); the smallest fe-
male found was 1.70 mm long (dissected live, July 1981:
the specimen had ripe ovaries, but no brood). The tran-
sition from male to female occurred over a broad size range,
with the majority of males less than 2.37 mm long (Table

1).

Seasonal Effects on Fecundity

An average (+SD) of 36 (+13) broods were counted
monthly (range = 15-56). Broods ranged in size from one
egg in each of three clams, 2.07, 2.29, and 2.37 mm in
length, to 327 embryos in a specimen 5.10 mm in length.
The smallest brooding female was 1.92 mm, and the largest
was 5.33 mm.

Females of all sizes were found with broods throughout
the year (Figure 2, Table 6). Broods contained uncleaved
eggs and embryos with and without shells. Uncleaved eggs
and the smallest embryos were held tightly together in
packets in the gills; older embryos were more loosely con-
nected to the rest of the brood. Eggs ranged from 0.21 to
0.26 mm in diameter. The largest embryos observed were
0.55 mm in shell length.

Fecundity was a linear function of adult size (Figure
2). The coefficients of determination (7?) for least-squares
regression were greater than 0.76 for all months except
March, August, and November 1981, when they were

Page 260

300
Fos)
°
°
ac
oO
= 200
7)
ro)
>
a
Pra
=
WwW
uw
ro)
rnd
Ww
@m 100
=
5
z
ay
<q
=
fo)
bE y)
WS 4
Y
fe) tLp/
1.5 2.5

The Veliger, Vol. 30, No. 3

JUN 8I

OCT 8I

SEP 81/ 8B
NOV 80
NOV 8I

DEC 8!
DEC "
AUG 8I
APR 8I
JAN 8I

MAR 8I
FEB 8I

3.5 4.5

FEMALE LENGTH (MM)
Figure 2

Seasonal change in the fecundity-size relationship of 7ransennella tantilla from the South Slough of Coos Bay,
Oregon. Each line is the best fit regression line for data analyzed by least squares. Slopes range from 30 to 113;
coefficients of determination (7?) range from 0.61 (August 1981) to 0.94 (December 1980) (P < 0.001 for all
regressions). The regression data were categorized into three seasonal groups (A, summer; B, fall; and C, winter-
spring) and compared by ANCOVA (P < 0.001). *Data for August 1981 were assigned to the summer group and

those for October 1980 to the fall group.

0.67, 0.61, and 0.69 respectively. All regressions were highly
significant (P < 0.001).

Fecundity was seasonally variable (Figure 2). Data col-
lected during the three seasons delineated in Figure 2 were
combined and compared by an analysis of covariance (AN-
COVA). Brood sizes of females of a given length were
significantly larger during summer months than during
late winter-early spring months and were intermediate in
size during fall months (ANCOVA, P < 0.001).

The seasonal change in brood size occurred in females
of all sizes and was similar during both years. Independent
comparisons of data collected during the same months (July,
October, November, and December of 1980 and 1981)
were made using ANCOVA. There were no significant
differences between any of the monthly pairs (P > 0.10).
An inconsistent depression in brood size during August
1981 could not be explained.

In all but two monthly samples from Coos Bay, 2-24%

M. A. Asson-Batres, 1988

Page 261

of the specimens examined had trematode sporozoites con-
taining cercariae attached to their gonadal tissue. Para-
sitized females were randomly matched with non-parasit-
ized females by shell length and collection date to correct
for animal size and seasonal effects on brood size. Regres-
sions of brood size on adult length for the resulting subset
of 75 pairs of females were compared by ANCOVA. The
brood sizes of animals with infected gonads were notably
depressed (uninfected clams: Brood Size = 68 x Adult
Length (mm) — 156, 7? = 0.53; infected clams: Brood
Size = 4 x Adult Length (mm) — 8; r? = 0.03; P < 0.001).
As a result, females with infected gonads were excluded
from the fecundity analyses above.

Release of Juveniles

Individual females (> 2.67 mm long) maintained in field
enclosures at Coos Bay released young during 11 of the
12 months they were monitored (Figure 3). Only two
females survived during October and neither released young.
The average (+SD) number of offspring released per fe-
male per month was 3 (+3) (ASSON-BATRES, 1982) which
is lower than might be expected given the number of em-
bryos known to be present in broods.

Periodic sediment burial and algal overgrowth led to
anoxia in some cages. The sediment within these cages
was black, indicating the presence of sulfide. Dead clams
had blackened shells that were still articulated. Broods of
dead eggs and shelled embryos were still present in dead
females from these cages.

After one to two months of field exposure, cages that
were sulfide-free mimicked the surrounding field com-
munity, with amphipods, cumaceans, tanaids, polychaetes,
nemerteans, and nematodes established in the cage sedi-
ment. After field exposure, clams in these cages were alive
except during October, when survivorship was inexplica-
bly low.

It is unlikely that unnatural cage conditions induced
females to release offspring because (1) shelled embryos
of release size were found in the body cavities of dead
females and (2) some living clams greater than 2.67 mm
long (presumably the majority of these clams were female,
see Table 1) did not release offspring (Figure 3). Thus,
while cage artifacts may have depressed release rates, the
results provide direct evidence that Transennella tantilla
can release young year-around.

Representative monthly size-frequency distributions of
Transennella tantilla collected from two of the South Slough
study sites are presented in Table 2A, B (data from the
other three sites are available in ASSON-BATRES, 1982).
The first size class, which includes clams 0.59-0.74 mm
in length, is underrepresented because the 500-um mesh
sieve did not retain newly released 7. tantil/a (the minimum
shell dimension, clam height, is less than 0.5 mm). Thus,
a lag of about one month exists between the actual time
of juvenile release and the time when clams of the smallest
size classes show up in the samples. As an example, the

100

80

60

% OF CAGES WITH OFFSPRING

Figure 3

Percent of caged females (>2.67 mm long) with offspring. Field
enclosures were maintained in the South Slough of Coos Bay,
Oregon, and monitored monthly during 1981. Only cages with
surviving females were examined for presence of offspring. The
total number of cages examined each month is indicated above
each bar.

majority of clams making up the second size class in the
samples collected at site PA during March and April were
probably released during February or March.

Juvenile clams were found at one or more sites during
every month. Because the absolute number of juveniles is
underrepresented in the sample (owing to the method of
collection, see above), the second size class (0.81-1.04 mm)
offers a better indication of the peak periods of juvenile
release (Table 2A, B; AsSON-BATRES, 1982). Taking the
lag period into consideration, peak release of juveniles
occurred at sites PA, MP, and MS during February through
April, and again at sites MP and MS during July and
August. Except for a single surge in release of young at
site PC during April, juvenile release was consistently low
at sites PB and PC throughout the study period.

Growth

Individual Transennella tantilla, retained in cages on the
Coos Bay mudflat, grew every month of the year (Table
3). The absolute change in shell length ranged from 0.07
to 0.56 mm per clam per month.

Distinct rings and zones were not present on the shells
of animals in monthly field collections, suggesting that shell
growth was continuous.

Mortality

A decline in the densities of large Transennella tantilla
occurred at sites MP, PA, and PB from June to September.
This is evident in Table 4, which compares the number
(or relative percent) of clams greater than 2.0 mm in shell

Page 262 The Veliger, Vol. 30, No. 3

Table 2

Size-frequency data for 7ransennella tantilla collected from two sites in the South Slough of Coos Bay, Oregon, during
1981. The number of clams comprising each size class are presented as percentages of the total number of clams present
in the 0.1-m* sample. Sample sizes are included at the bottom of the table so that raw numbers can be generated, if

desired.

Part A. Site PA

Size class (mm) Mar Apr May Jun Jul Aug Sep Oct Nov Dec
0.59-0.74 2 1 1 0.7 0.5 0.4 0.7 0.6
0.81-1.04 51 48 23 24 21 12 5 4 20
1.11-1.33 29 25 44 33) 23 23 11 4 7 8
1.41-1.63 8 11 22 31 37 26 19 7 1 2
1.70-1.92 4 6 7 10 17 27 26 19 3 6
2.00-2.22 2 3 2 0.7 3 11 23 30 8 13
2.29-2.52 2 3 1 0.5 1 14 20 24 19
2.59-2.81 0.8 1 0.4 1 11 23 13
2.89-3.11 0.2 1 0.3 0.2 4 11 14
3.18-3.40 0.5 0.3 0.4 0.7 13 4
3.48-3.70 0.3 3 0.6
3.77-4.00 0.3 0.1 0.1 0.2 7
4.07-4.29 0.2 0.1 1

Total number of clams
in sample 593 UN 1018 410 342 376 203 152 75 158
Part B. Site MP

Size class (mm) Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
0.59-0.74 0.2 4 2 0.7 6 6 1 0.5 0.3 0.2
0.81-1.04 27 11 43 35 19 32 62 43 13 8 1
1.11-1.33 18 10 16 30 26 Zl 15 35 22 5 19
1.41-1.63 19 14 9 10 Bil 20 7 13 26 14 22
1.70-1.92 11 LY 9 6 13 10 5 5 21 Bil 20
2.00-2.22 12 24 8 6 5 3 3 2 9 24 13
2.29-2.52 6 14 6 5 3 1 1 1 4 14 5
2.59-2.81 4 5 3 2 2 1 0.5 0.6 2 5 3
2.89-3.11 1 2 1 2 2 0.6 0.2 1 3 0.8
3.18-3.40 0.2 0.7 0.7 1 1 0.3 0.3 0.8 0.7
3. 48-3.70 0.8 0.7 0.1 0.4 0.7 0.5 0.3
3.77—4.00 0.2 0.7 0.1 0.1
4.07-4.29 0.2 0.1
4.37-4.59 0.1 0.1

Total number of clams
in sample 479 606 1418* 1355 1524 1163 929 1042 663 600* 1147

* Estimate based on two subsamples of 0.03 m? each.

length in monthly samples from the sites. Pre-decline den-
sities of large clams were re-established at the sites during
fall and winter months. Clams less than 2.0 mm in shell
length did not decline during the summer at sites MP, PA,
and PB (data not shown).

There was a precipitous decline in all sizes of Transen-
nella tantilla at site PC in May (ASSON-BATRES, 1982).
During June and July, repeated samples were checked for
the presence of 7. tantilla, but specimens retained by the
500-um mesh screen were not present. Concomitant with
the disappearance of live 7. tantilla from the site was the
appearance of numerous 7. tantilla half-shells and shell
fragments. Clams greater than 2.0 mm in shell length did
not reach pre-decline densities at site PC (Table 4). A

year later (June 1982), numerous (>10) samples were
sieved (500-~m mesh) at the site and only one living 7.
tantilla was found. Such intensive sieving before the crash
would have retrieved hundreds of clams visible to the naked
eye.

Neither large (Table 4) nor small 77ransennella tantilla
declined in number at site MS during summer months.

Life-History Characteristics of
Transennella tantilla from False Bay

Fecundity was a linear function of adult size and was
seasonally variable (Table 5). Females of a given size in
False Bay had smaller broods than females of comparable
size in Coos Bay and, although females in False Bay reached

M. A. Asson-Batres, 1988

Table 3

Growth of Transennella tantila retained in field enclosures
in the South Slough of Coos Bay, Oregon, during 1980-
1981. One clam present per cage.

% of
Number of survivors

Month(s) of Change in length

exposure survivors that grew (mm) mean + SD*
Dec-Feb 29 66 0.12 + 0.06
Jan 54 72 0.11 + 0.06
Jan-Mar De) 65 0.13 + 0.06
Feb 26 15 0.06 + 0.02
Feb-Apr 25 88 0.16 + 0.10
Mar 48 75 0.11 + 0.06
Mar-—May 28 SY 0.25 + 0.20
Apr 66 53 0.15 + 0.08
Apr-Jun 4 WS 0.30 + 0.20
May 69 38 0.12 + 0.08
May-Jul 11 55 0.23 + 0.10
Jun 21 48 0.11 + 0.04
Jul 34 59 0.18 + 0.14
Aug 26 81 0.12 + 0.06
Sep 33 7 0.10 + 0.04
Oct 4 75 0.12 + 0.04
Nov 46 80 0.17 + 0.08
Dec 42 if 0.07 + 0.00
* The mean includes only those clams that showed an increase
in length.

larger sizes than females in Coos Bay, the maximum brood
sizes of False Bay animals were smaller than those of Coos
Bay females during four of the six months sampled (Table
6).

Of the clams from the bimonthly collections from False
Bay 2-17% were infected with trematode parasites. Par-
asitized females had significantly reduced brood sizes (AN-
COVA, P < 0.001) and were excluded from the fecundity
analyses.

Table 4

Number (%) of Transennella tantilla greater than 2.0 mm

in shell length in monthly samples collected from each of

the five study sites in the South Slough of Coos Bay, Or-
egon, in 1981.

Month PC PA PB MP MS
Feb 198 (34) — 44 (51) 116 (24) 38 (28)
Mar 229 (49) 37 (6) 71 (49) 285 (47) 68 (15)

Apr 266(48) 100(9) 422(69)* 267(19) 47 (7)

May 3 (2) 43 (4) 41 (59) 226 (17) 44 (7)
Jun 0 (0) 7 (2) 8 (24) 212 (14) 82 (18)
Jul 0 (0) 10 (3) (a@)) 69 (6) 167 (27)
Aug 4 (7) 45 (12) 4 (3) 45 (5) 57 (27)
Sep Zia 73) 77 (38) 40 (49) 37 (4) 62 (11)
Oct 18 (83) 100 (66) 62 (67) 108 (16) 93 (24)
Nov 50 (94) 62 (82) 46(49) 284 (47) —

Dec 25 (80) 100(64) 47(30) 263(23) 133 (38)

* The April sample size was spuriously high because the sam-

ple was collected from the slope by a pier where wave action
deposited large individuals of 7. tantilla.

Page 263

Table 5

Brood size of Transennella tantilla collected from False Bay

on San Juan Island, Washington. Regression data are for

brood size (B) plotted over adult length (L) (P < 0.001
for all regressions).

Date De Equation r
Nov ’80 31 B = 77L — 263 0.77
Feb ’81 36 B = 20L — 62 0.85
Apr ’81 65 B = 30L — 90 0.72
May ’80 Bil B = 41L — 128 0.64
Jun 81 48 = 67L — 202 0.89
Aug 781 48 B = 82L — 303 0.85
Oct ’81 39 B = 37L — 127 0.55

* n indicates the number of animals examined.

DISCUSSION

The field enclosure studies provide direct evidence that
Transennella tantilla can reproduce and grow year-around
in the South Slough of Coos Bay, Oregon. The results
from monthly field samples support these observations.
The presence of juvenile clams in all field collections sup-
ports the contention that release is continuous. Because it
is known that variations in growth rate are recorded by
distinct zones or rings on bivalve shells (NAYAR, 1955;
JONEs, 1983), the absence of such rings on the shells of
T. tantilla in this location suggests that growth is contin-
uous.

Continuous release of young by 7ransennella tantilla is
not exceptional; other bivalves in northern waters also
spawn year-around. Mytilus californianus spawns all year
off the west coast of the United States (WHEDON, 1936;
SUCHANEK, 1981) and at least part of the populations of
Astarte borealis and A. elliptica in the Baltic Sea carry eggs
and sperm year-around and spawn for a period of up to
eight months (VON OERTZEN, 1972).

A majority of the clams between 1.85 and 2.37 mm in
shell length from the sites in South Slough were males,
whereas larger animals were predominantly females (Ta-
ble 1). These results, along with HANSEN’s (1953) dem-
onstration (using histological techniques) that some indi-
viduals were in the process of a sex reversal, provide strong
support for protandry in this species. The sex structure of
the population was similar throughout the year at all sites,
which suggests that sex reversal occurs throughout the
year. The male-to-female sex ratios of populations sampled
at sites PA and PB were 55:45 and from sites MP and
MS were 61:39 (AssON-BATRES, 1982). The proportion
of males at each site is probably an underestimate because
many animals smaller than the cut-off length of 1.85 mm
likely were males.

Protandry is predicted when reproductive success is in-
dependent of size for males, but proportionally greater for
large females than for small ones (GHISELIN, 1969;
WARNER, 1975). Model simulations that assume these con-
ditions predict that the smallest mature individuals in a

Page 264

Table 6

Comparison of the mean (x) brood size of Transennella
tantilla by shell length (mm), month, and geographic lo-
cation. The number (n) of animals examined is indicated.
The animals were collected from False Bay on San Juan
Island, Washington, and the South Slough of Coos Bay,

Oregon.
Female
size
class Helse IEE) =e Coes Bey
Month (mm) x (n) x (n)
Nov ’80 2-3 = = 24 (5)
3-4 31 (8) 74 (9)
4-5 74 (11) 127 (4)
5-6 150 (12) — —
Feb °81 2-3 — — 11 (16)
3-4 9 (17) 32 (24)
4-5 Di (19) 56 (4)
5-6 = = 88 (3)
Apr 781 D=S} 3 (2) 20 (15)
3-4 10 (25) 51 (32)
4-5 37 (30) 96 (8)
5-6 85 (8) = —
Jun ’81 D=3) 1 (6) 35 (26)
3-4 12 (10) 150 (19)
4-5 92 (12) 265 (5)
5-6 169 (15) 275 (1)
6-7 185 (5) Be =
Aug ’81 D8 ae — 15 (20)
3-4 6 (18) 53 (16)
4-5 26 (17) 129 (1)
5-6 145 (11) = ss
6-7 232 (2) = me
Oct 81 2-3 = — 20 (6)
3-4 21 (2) 73 (21)
4-5 39 (29) 143 (1)
5-6 61 (8) = =a

population will be male. At some larger size, it will be
more profitable to be female and, at this point, a change
in sex will occur. Field studies of protandrous shrimp and
plants offer evidence that the model is realistic (CHARNOV,
1979; POLICANSKY, 1981). Because large females of T7an-
sennella tantilla produce proportionally more embryos than
small females, it is tempting to speculate that the model
offers an appropriate explanation for protandry in this
species. It is of interest that Gemma gemma, also a small
(5 mm, maximum shell length) brooding venerid is dioe-
cious. Female G. gemma begin brooding at about 2.0 mm
in length, and fecundity increases logarithmically with
female size. Juveniles are released when they are fully
developed. Their life-span is thought to be 2 yr (SELLMER,
1967; GREEN & Hopson, 1970). Although a positive cor-
relation between fecundity and female size exists in both
species, 7. tantilla is a sex-changer and G. gemma is not.
It is currently not possible to test the relative interspecific
productivity of males. It may be that reproductive success

The Veliger, Vol. 30, No. 3

is size-dependent for male G. gemma and size-independent
for male 7. tantilla.

The summer decline in densities of Transennella tantilla
from four of the five study sites in Coos Bay was most
likely due to predation. Juvenile Cancer magister (Dana)
(13-30 mm in carapace width) forage for 7. tantzlla in the
South Slough of Coos Bay, Oregon (AssON-BATRES, 1986).
When feeding on the clams, this crab characteristically
separates the valves, leaving one half-shell intact
(ASSON-BATRES, 1986). The megalops of C. magister were
present in the Coos Bay estuary from mid-March to the
end of May of 1981 (ROWELL, 1981) and would have
metamorphosed to first instar juveniles throughout April
to June. The coincidental disappearance of the clams and
appearance of juvenile C. magister, and the concomitant
appearance of half-shells and shell fragments at the site
where the clams were found when alive, suggest that ju-
venile C. magister was a factor in the summer decline of
T. tantilla. In support of this interpretation, it has been
reported that small bivalves are a major part of the diet
of first year C. magister (STEVENS et al., 1982).

Shore birds and bottom-feeding fish that appear sea-
sonally may have also contributed to the decline of Tran-
sennella tantilla. OBREBSKI (1968) indicated that the gut
contents of unidentified shore birds collected near Bodega
Bay contained Transennella. VIRNSTEIN (1977) reported
that spot fish, Lezostomus xanthurus, were important pred-
ators on juvenile clams (1-3 mm, shell length) in the York
River of Chesapeake Bay. Whether birds or fish feed sea-
sonally on 7. tantilla in South Slough has not been inves-
tigated. Juveniles of other species of crabs may have also
preyed on 7. tantilla during the summer, but none are
likely to have been as abundant as juvenile C. magister.

The population decline of the large size classes at three
of the five sites, and the population crash of all sizes at
one site, suggest that mortality may be unpredictable for
this species. Direct release of relatively immobile young
can lead to the formation of groups of animals separated
in space (patches). This could provide a refuge from pred-
ators, as they may overlook a prey patch. The stable pop-
ulation density observed at site MS during this study,
concurrent with the decline of population densities at other
sites, is consistent with such a prediction.

Individuals of Transennella tantilla from False Bay reach
lengths up to 1.3 mm longer than their conspecifics in Coos
Bay (Table 7). According to Gray (1978), 7. tantilla in
Tomales Bay, California (38.4°N) reach 7.00 mm in length.
Thus, the size of 7. tantilla at False Bay, Coos Bay, and
Tomales Bay is not correlated with the change in latitude.

Transennella tantilla is conspicuously distributed over
much of the tideflat in False Bay. At mean lower low
water, where the species is most dense in False Bay, it is
a numerically dominant species (PAMATMAT, 1969;
BRENCHLEY, 1981). In contrast, 7. tantzlla is smaller, less
exposed, and distributed in isolated patches on the mudflat
in the South Slough of Coos Bay, giving the impression

M. A. Asson-Batres, 1988

Page 265

Table 7

Comparisons of life-history traits of 7ransennella tantilla from False Bay on San Juan Island, Washington, and the South
Slough of Coos Bay, Oregon. Observations are personal except as indicated in parentheses. AB = AssON-BATRES, 1982;
H = Hansen, 1953.

False Bay, Washington

Latitude 48.5°N
Shell length

Male size range
Female size range

Female reproductive behavior

>2.80 mm

Maximum brood size (adult length)
Diameter of uncleaved egg in brood chamber
Juvenile release size

that it is less abundant there than in False Bay. If abun-
dance is greater in False Bay than in Coos Bay, it is not
a result of increased brood sizes: females of similar size
brood fewer embryos in False Bay than in Coos Bay (Ta-
bles 6, 7).

Females in both locations produce eggs of similar size
(Table 7), but in False Bay, young are released at a larger
size. The energetic costs of producing offspring should be
equal at the two locations, if, as it is assumed (HANSEN,
1953), embryos receive no nutrition from the parent during
development. In this species, then, egg size appears ge-
netically fixed, whereas other life-history traits are more
plastic.

Parasitized animals from Coos Bay and False Bay had
significantly smaller brood sizes. KABAT (1984) reported
that 31% of the brooding females he examined from False
Bay hosted parasites and produced only 40% as many
embryos as non-parasitized females of the same size. In
this study, the percentage of clams infected with gonad
trematodes was extremely variable: 0-24% of the speci-
mens collected at Coos Bay, and 2-17% of those from False
Bay had parasitized gonads. There was no apparent cor-
relation between the number of parasitized animals and
the collection date (personal observation, unpublished).

Factors that restrict the productivity of female Transen-
nella tantilla in Coos Bay and False Bay are the animal’s
life-span, the incidence of parasitism, and seasonal effects
on egg production, embryonic growth, and juvenile release.
Senility does not limit productivity because all non-par-
asitized, mature females are found with broods, and the
oldest (largest) females have the largest broods. It is un-
certain whether the allometry of egg production and brood-
ing (STRATHMANN & STRATHMANN, 1982) limits produc-
tivity in T° tantilla. The linearity of the correlations between
brood size and female size (recall that wet weight is cor-
related with length, see Results above) and the capacity
of the organism to adjust its brood size upward during
some seasons suggest that large 7. tantilla have ample space

0.65-6.60 mm
1.50-4.60 mm (H)

Brood present all year; fecundity a
linear function of size

293 (5.6 mm)

0.25 mm (H, AB)

0.65 mm (H, AB)

Coos Bay, Oregon

43.8°N

0.55-5.30 mm

<1.85-3.48 mm

>1.70 mm

Brood present all year; fecundity a
linear function of size

327 (5.1 mm)

0.21-0.26 mm

0.53-0.55 mm

to brood as many gametes as they are capable of producing.
However, differences in the brood structures of animals
from Coos Bay and False Bay may argue against this
interpretation; a limitation in brood space could constrain
females to brood either higher numbers of small young (as
in Coos Bay) or lower numbers of large young (as in False
Bay).

In summary, 77ansennella tantilla is a small, protandric,
brooding bivalve that grows and reproduces year-around
in the South Slough of Coos Bay, Oregon. It appears to
be subject to intense seasonal predation by incoming set-
tlements of juvenile Cancer magister and possibly shore
birds and bottom-feeding fish. Maximum adult size is geo-
graphically variable, but there does not appear to be a
correlation between animal size and latitude. Brood size,
juvenile release size, age at maturity, and the size range
of males and females vary between geographic sites (Table
7). Whether the comparative flexibility observed in many
of the life-history characteristics of this species (Table 7)
represents genetic differences or physiological adaptability
to locally induced pressures has not been investigated. In
this regard, a reciprocal transplant experiment and elec-
trophoretic comparative analysis of the populations would
be of interest.

ACKNOWLEDGMENTS

I thank P. W. Frank for encouragement and advice
throughout the study and for assistance with preparation
of the manuscript; R. R. Strathmann and R. I. Ingermann
for helpful discussions; P. Rudy, Director of the University
of Oregon Institute of Marine Biology, E. Kozloff, Acting
Director of Friday Harbor Laboratories, and their staff
for providing research facilities; and S. Batres for assistance
in the design and construction of the experimental field
cages. The field research was partially funded by a grant-
in-aid from Sigma Xi. Preparation of the manuscript was
supported in part by PHS Research Grant HD 15308.

Page 266

LITERATURE CITED

ASssON-BaTRES, M. A. 1982. The life history traits and pop-
ulation dynamics of the brooding bivalve, Transennella tan-
tilla (Gould) in the South Slough of Coos Bay, Oregon.
Master’s Thesis, University of Oregon, Eugene. 73 pp.

ASSON-BaTRES, M. A. 1986. The feeding behavior of the ju-
venile Dungeness crab, Cancer magister on the bivalve, Tran-
sennella tantilla (Gould), and a determination of its daily
consumption rate. Calif. Fish Game 72:144-152.

BRENCHLEY, G. A. 1981. Disturbance and community struc-
ture: an experimental study of bioturbation in marine soft-
bottom environments. Jour. Mar. Res. 39:767-790.

CuHarRNov, E. L. 1979. Natural selection and sex change in
pandalid shrimp: test of a life history theory. Amer. Natur.
113:715-734.

CHARNOV, E. L. 1982. The theory of sex allocation. Princeton
University Press: Princeton. 355 pp.

CHRISTIANSEN, F. B. & T. M. FENCHEL. 1979. Evolution of
marine invertebrate reproductive patterns. Theor. Pop. Biol.
16:267-282.

GHISELIN, M. T. 1969. The evolution of hermaphroditism
among animals. Quart. Rev. Biol. 44:189-208.

GouLpD, A. A. 1852. Descriptions of shells from the Gulf of
California and the Pacific coasts of Mexico and California.
Bost. Jour. Natur. Hist. 6:374-408.

Gray, S. 1978. Comparative anatomy and functional mor-
phology of two species of Transennella (Bivalvia: Veneridae).
Master’s Thesis, San Francisco State University, San Fran-
cisco. 68 pp.

Gray, S. 1982. Morphology and taxonomy of two species of
the genus Transennella (Bivalvia: Veneridae) from western
North America and a description of 7. confusa sp. nov. Mala-
col. Rev. 15:107-117.

GREEN, R. H. & K. D. Hopson. 1970. Spatial and temporal
structure in a temperate intertidal community, with special
emphasis on Gemma gemma (Pelecypoda: Mollusca). Ecol-
ogy 51:999-1011.

HANSEN, B. 1953. Brood protection and sex ratio of Transen-
nella tantilla (Gould), a Pacific bivalve. Vidensk. Medd. fra
Dansk naturh. Foren. 115:313-324.

Jones, D. S. 1983. Schlerochronology: reading the record of
the molluscan shell. Amer. Sci. 71:384-391.

KapaT, A. R. 1984. Brooding, parasitism, and reproductive
output in Transennella tantilla (Bivalvia). Amer. Zool. 24:
14A (abstract).

KEEN, A. M. 1937. An abridged checklist and bibliography of
west North American marine Mollusca. Stanford University
Press: Stanford. 87 pp.

The Veliger, Vol. 30, No. 3

MenGE, B. A. 1975. Brood or broadcast? The adaptive sig-
nificance of different reproductive strategies in the two in-
tertidal sea stars Leptasterias hexactis and Pisaster ochraceus.
Mar. Biol. 31:87-100.

NarcuHI, W. 1970. The presence of byssus in adults of T7ran-
sennella tantilla (Gould) (Bivalvia: Veneridae). Wasmann
Jour. Biol. 28:233-236.

Nayar, N. N. 1955. Studies on the growth of the wedge clam,
Donax (Latona) cuneatus Linnaeus. Ind. Jour. Fish. 2:325-
348.

OBREBSKI, S. 1968. On the population ecology of two intertidal
invertebrates and the paleoecological significance of size-
frequency distributions of living and dead shells of the bivalve
Transenella [sic] tantilla, Ph.D. Thesis, University of Chi-
cago, Chicago. 102 pp.

PAMATMAT, M. M. 1969. Seasonal respiration of Transennella
tantilla Gould. Amer. Zool. 9:418-426.

PHILLIPS, D.S. 1978. Basic statistics for health science students.
W. H. Freeman & Co.: San Francisco. 185 pp.

POLICANSKY, D. 1981. Sex choice and the size advantage model
in jack-in-the-pulpit (Arisaema triphyllum). Proc. Natl. Acad.
Sci. USA 78:1306-1308.

ROWELL, D. L. 1981. The dispersal of Cancer magister larvae
in the Coos Bay estuary. Master’s Thesis, University of
Oregon, Eugene. 66 pp.

SELLMER, G. P. 1967. Functional morphology and ecological
life history of the gem clam Gemma gemma (Eulamellibran-
chia: Veneridae). Malacologia 5:137-223.

STEVENS, B. G., D. A. ARMSTRONG & R. CUSIMANO. 1982.
Feeding habits of the Dungeness crab Cancer magister as
determined by the index of relative importance. Mar. Biol.
72:135-145.

STRATHMANN, R. R. & M. F. STRATHMANN. 1982. The re-
lationship between adult size and brooding in marine in-
vertebrates. Amer. Natur. 119:91-101.

SUCHANEK, T.H. 1981. The role of disturbance in the evolution
of life history strategies in the intertidal mussels Mytilus
edulis and Mytilus californianus. Oecologia 50:143-152.

VIRNSTEIN, R. W. 1977. The importance of predation by crabs
and fishes on benthic infauna in Chesapeake Bay. Ecology
58:1199-1217.

VON OERTZEN, J. A. 1972. Cycles and rates of reproduction of
six Baltic Sea bivalves of different zoogeographical origin.
Mar. Biol. 14:143-149.

WarNER, R. R. 1975. The adaptive significance of sequential
hermaphroditism in animals. Amer. Natur. 109:61-82.
WHEDON, W. F. 1936. Spawning habits of the mussel Myézlus
californianus Conrad with notes on the possible relation to

mussel poison. Univ. Calif. Publ. Zool. 41:35-44.

The Veliger 30(3):267-277 (January 4, 1988)

THE VELIGER
© CMS, Inc., 1988

Aspects of the Life History and Population Biology of

Notospisula trigonella (Bivalvia: Mactridae) from

the Hawkesbury Estuary, Southeastern Australia

by

A. R. JONES anp A. MURRAY

Division of Invertebrates, The Australian Museum, P.O. Box A285, Sydney, 2000, Australia

AND

G. A. SKILLETER

School of Biological Sciences, University of Sydney, N.S.W. 2006, Australia

Abstract.

Aspects of the life history of Notospisula trigonella and spatial and temporal variations in

its abundance in the Hawkesbury Estuary, New South Wales, are described and related to physico-
chemical factors. Sexes were separate with a sex ratio close to 1:1. Spawning usually occurred between
August and November but sometimes continued until February. Annual variation in the timing of onset
and duration of spawning occurred and the nature of spawning cues is unclear. Recruitment always
occurred between August and November, usually with a single cohort that appeared to survive about
1 yr. Growth rates were usually highest between November and February when cohorts of small size
were present.

Spatial differences in abundance were usually significant but variable. The species was absent from
salinities less than 10%o and usually rare at sites closest to the ocean, where mean low-water salinities
were 31.4%. Water depth and sediment grade had little apparent effect on abundance as differences
associated with the former were inconsistent and those with the latter were not significant. Temporal
differences were somewhat cyclic in the middle estuarine reaches, with maximum abundance in No-
vember, but were variable in the lower reaches. Abundance fell to zero following a major flood. Much

of the variability observed may ultimately be due to the unpredictable rainfall of the region.

INTRODUCTION

Notospisula trigonella (Lamarck, 1818) is a suspension-
feeding mactrid bivalve found in estuaries and coastal waters
of all Australian states (WILSON & KENDRICK, 1968). It
inhabits a wide range of sedimentary habitats (ROBINSON
& GIBBs, 1982) and can dominate the macrofaunal com-
munity with densities exceeding 2000 m~? (GREEN, 1968).
Despite this, little is known about its life history and pop-
ulation biology. Available information is limited to a study
of mortality (where it was called N. parva) by GREEN
(1968), fragmentary notes in several benthic community
studies (¢.g., CHALMER et al., 1976; STEPHENSON et al.,
1977; RAINER & FITZHARDINGE, 1981; POORE, 1982) and
STEJSKAL (1985).

This paper is based on information collected during a
long-term study of the macrobenthic community of the
Hawkesbury River estuary in southeastern Australia. Be-
cause it was the dominant species in the study, the biology
of Notospisula trigonella is treated here separately from the
rest of the fauna. The aims are to describe aspects of the
life history (reproductive cycle, sex ratio, recruitment, and
growth) and population biology (spatial and temporal dis-
tributions) in relation to physicochemical factors.

MATERIALS anpD METHODS
Field Sampling

Twelve across-estuary transects containing 29 sampling
sites were located between the mouth of the Hawkesbury

Page 268

Table 1

Mean values for depth, mean grain size (M,), % mud, and
bottom-water salinity (adjusted to low-water values) for
most sites over the first five samplings (summer 1977 to
summer 1978 inclusive). The sites upstream of 9.1 and
9.2 included both deep and shallow sites on each transect
and all had sediments with <20% mud. Salinities de-
creased from 7.3%o at transect 10 to <0.5%o at transect 14.
Site 7A was 20 m deep with muddy sand sediments and
salinity similar to site 7.1.

Depth M, Mud Salinity
Site (m) (o) (%) (Yoo)
1.1 4 6.0 59 31.4
1.3 10 4.4 31 31.4
Zoi 4 6.1 61 29.7
Det 5 6.0 60 29.7
2.3 12 Toll 88 29.7
3.1 12 5.4 49 27.9
32 6 3.1 17 OS)
3.3 5 8.1 93 PD)
6.2 8 4.4 36 24.0
6.3 8 lod 6 24.0
Toil 12 Del 51 20.5
V2 8 Desk 13 20.5
(ES 6 7.6 83 20.5
8.1 6 6.0 Sy 16.8
8.2 16 3.4 17 16.8
Oe 20 6.2 63 11.8
O22. 6 3.0 20 11.8

Estuary and its junction with the Colo River (Figure 1).
Sites on most transects varied in depth and sediment grade
(Table 1). Samples were taken every season, with summer,
autumn, winter, and spring being represented by Febru-
ary, May, August, and November respectively. All sites
were sampled from February 1977 until February 1978
inclusive. Sampling was continued seasonally at sites 3.1
and 3.2 until spring (November) 1979 (z.e., 3 yr total) and
at sites 1.1, 1.3, 2.1, 2.2, 7.1, and 7.2 until summer (Feb-
ruary) 1984 (z.e., 7 yr total). No samples were taken at
sites 1.3, 2.1, and 2.2 in autumn 1980 owing to equipment
malfunction. Each sample comprised four 0.05-m? Smith-
McIntyre grabs and material retained on a 1-mm sieve
was preserved in buffered 10% formalin for subsequent
laboratory processing under stereomicroscopes.

The salinity and temperature of bottom water were
measured by a Goldberg temperature-compensated re-
fractometer, a mercury thermometer (using water obtained
by a closing water bottle), and a Martek Mark V in situ
water quality analyzer whose sensors were lowered to the
bottom. Sediment samples were taken from an additional
grab taken at each time and site until autumn 1981. The
sieve and pipette procedures of FOLK (1974) were used to
analyze the grain size composition of the sand and silt-
clay components respectively. River-discharge data were
obtained from the New South Wales Metropolitan Water

The Veliger, Vol. 30, No. 3

Sewerage and Drainage Board’s gauging station at Penrith
upstream of the tidal limit.

Life History

In summer 1980, a dense population was discovered at
site 7A (Figure 1) from which one or two grabs were
collected every three months until spring 1983. Specimens
from this site were used to describe the reproductive cycle
and estimate sex ratios, recruitment, and growth. The
minimum reproductive size was determined for specimens
from sites 7A, 7.1, 7.2, 2.1, and 3.1.

The interval between sampling (three months) was im-
posed by the logistics of a long-term community study and
is greater than would normally be used for accurate de-
scriptions of reproductive cycles. However, it is possible
to gain considerable insight into the reproductive cycle by
considering seasonal reproductive changes in conjunction
with size-frequency distributions and by relating periods
of spawning to those of recruitment (ROBERTS, 1984).

Fifteen individuals of 8 to 15 mm shell length were
selected from each sample from site 7A and tissue speci-
mens were prepared for histology. The gonadal portion of
the visceral mass was removed and dehydrated in graded
alcohols, cleared in xylene, embedded in paraffin wax,
sectioned at 7-wm intervals, and stained with Harris’
hematoxylin and eosin (CARLETON, 1957). At least 20
serial sections from each specimen were examined micro-
scopically. Determination of the stage of gametogenesis
was based on the classifications of BRALEY (1984) and
ROPES (1968): z.e., stage O—resting or spent gonad; stage
{—early active; stage 2—late active; stage 3—ripe; stage
4—partially spawned; stage 5—spent. Allocation to a par-
ticular stage was made if more than 75% of the follicles
showed this level of development.

Sex ratios and the minimum reproductive size were
determined histologically and by observing the external
condition (color) of the gonad in ripe individuals (stage 3).
At other stages of gametogenesis, the color of the gonad
could not be used to determine gender. In order to deter-
mine the minimum reproductive size, specimens ranging
in size from 2 to 17 mm were examined for the presence
of ripe gonad. Squash mounts of the gonad region of the
visceral mass were used as a final check for small individ-
uals without externally visible gonad.

Size Structure and Growth

Shell lengths of 200 randomly selected individuals from
each sample taken at site 7A were measured with vernier
calipers (+0.1 mm) and placed into 1-mm size classes. For
samples with less than 200 specimens, all available indi-
viduals were measured. Estimates of mean cohort size from
size-frequency distributions were made using normal
probability paper (Cassig, 1954). Growth rates were then
estimated from the displacement of the mean length of
those cohorts that were clearly recognizable and could be
followed through time.

A. R. Jones ef al., 1988 Page 269

Pacific Ocean

HAWKESBUR
RIVERS Tie.
Patonga C a0 eo

= 7
Mullet Ck Ly

to Cowan Ck
aS
y una¢

Berowra Ck

Mangrove =
7, NK
S

S
S

1

HAWKESBURY
RIVER

11-2

Macdonald
R

Figure 1

Map of Hawkesbury River estuary showing location of sampling sites. The transect number is indicated by the
left hand numeral.

Page 270

Data Analysis

Analyses of the relationship between the abundance of
Notospisula trigonella and several abiotic variables (distance
from the river mouth, water depth, sediment grade, season,
year, river discharge, salinity, and temperature) were done.
Some of these were confounded, e.g., salinity varied with
distance from the river mouth and sediment grade varied
with both distance from the mouth and depth.

Differences in abundance associated with those variables
whose levels could be fixed (distance from the river mouth,
water depth, sediment grade, season, and year) were iden-
tified by analysis of variance (ANOVA) in various factorial
combinations (see below) and a posterior: Student-New-
man-Keuls (SNK) multiple comparisons. Cochran’s test
was used to test for variance heterogeneity and variance-
stabilizing transformations were used where necessary.
These ANOVAs deal with both spatial and temporal as-
pects of distribution and abundance.

Different spatial patterns during the first five sampling
times were determined in the following ways. Patterns
associated with distance from the mouth (along-estuary
patterns) and depth (across-estuary patterns) arose from
the transects containing both deep (>10 m) and shallow
(3-6 m) sites. These data were analyzed by three-way
fixed-factor ANOVAs (6 along-estuary positions x 2
depths x 5 times). Patterns associated with different sed-
iments were identified by subjecting abundance data from
transect 6 to a two-factor (sediment type x time) ANOVA.
Only at transect 6 were sediment differences not confound-
ed by depth differences. All the above ANOVAs included
a time factor in order to assess the repeatability of various
spatial differences in abundance.

Temporal patterns at transects with long-term data
available (7 yr for transects 2 and 7) were analyzed by
three-way fixed-factor ANOVAs (site X season X year).
Year was considered a fixed factor because all available
years were sampled. This fixed-factor model restricts in-
ferences to the paricular sites, seasons, and years involved.

Relationships between abundance and those abiotic
variables whose levels could not be fixed (temperature,
salinity, and river discharge) were quantified using Spear-
man rank correlations and partial correlations. The latter
provided statistical control for confounded variables, 2.e.,
the association between abundance and salinity (for ex-
ample) could be quantified independently of the association
with temperature and river discharge.

RESULTS

Physicochemical Characteristics of Sampling Sites

Considerable variation in physicochemical characteris-
tics occurred. The mean salinity of bottom water varied
from 31.4%o at transect 1 to 11.8%o0 at transect 9 (Table
1). No specimens of Notospisula trigonella were obtained
in the lower salinities upstream of transect 9. There were
temporal variations in salinity which were largely caused

The Veliger, Vol. 30, No. 3

by a major flood in March 1978, minor floods in March
1977 and June 1978, and a major drought from 1979 until
1981 (Figure 2). Recorded temperature of bottom water
at site 7A varied from 25.7 to 14.4°C. The range was
approximately 2°C greater and less in the upper (transects
11-14) and 2°C less in the lower (transects 1-3) reaches
respectively. The finest and coarsest sediments were located
in the lower and upper reaches respectively, and sediment
grade varied substantially across the estuary at transects
3-9 (Table 1).

Sex Ratio and Minimum Reproductive Size

Notospisula trigonella has separate sexes and the popu-
lation at site 7A displayed a sex ratio of 1:1.05 (male:
female, n = 240) which is not significantly different from
1:1 Q&? = 0.15, P > 0.05). No hermaphrodites were ob-
served.

The minimum recorded shell length of reproductively
mature individuals at site 7A was 5 mm. However, at sites
7.1, 7.2, 3.1, and 2.1, it was only 3-4 mm.

Spawning and Recruitment

Spawning, as indicated by the presence of partially
spawned individuals, usually occurred in November and
sometimes continued until February of the following year
(Figures 3A-D). However, the timing of both the onset
of spawning and its duration appeared to vary among
years. For example, in 1981, partially spawned specimens
(stage 4) were present in August, whereas in 1983 and
1982, this stage was not observed until November and the
following February respectively (Figures 3B-D). Fur-
thermore, spawning had probably concluded by February
in 1981 and 1982 but was continuing during February of
1980 and 1983. In fact, the presence of spent individuals
as late as May in 1980 implies an exceptionally long
duration for the spawning period starting in 1979 (Figure
3A).

Recruitment of a new cohort always occurred between
August and November but variability in the number of
cohorts per year among years was apparent (Figure 4). In
1982 for example, cohort 4 had settled prior to the August
sampling and was supplemented by cohort 5, which had
settled prior to the November sampling (Figures 4K, L).
Each cohort appeared to survive about 1 yr, except cohort
4, which suffered high early mortality (Figures 4L, M).
Although spawning in 1980 and 1983 continued until Feb-
ruary (Figures 3A, D), no recruitment ensued (Figures
4A-C, M-O), although specimens too small to be sampled
may have settled temporarily.

Growth

In all years except 1982, growth rates showed a single
peak between November and February. In 1982, growth
rates peaked in this period and also between August and
November when settlement (cohort 4) occurred earlier than

A. R. Jones et al., 1988

Page 271

LOG, RIVER DISCHARGE ( MI.)
oo > on oOo

ss | Sc)
a
= (0)
w
= 2:5
p=)
(=)
=
= 2-0
ras}
o 1:5
=—
=—
as
= 1-0
0:5
0

FMANFMANFMANFMAN FMANFMAN FMAN
1977 1978 1979

1980 1981 1982 1983

Figure 2

Temporal distribution (1977-1983 inclusive) of mean number of individuals per grab at sites 2.1 (@), 2.2 (O), 7.1
(¥), and 7.2 (VY). Standard errors are omitted for clarity but varied from 0.0 to 0.5 (2.1), 0.0 to 0.6 (2.2), 0.0 to
0.6 (7.1) and 0.0 to 0.8 (7.2) following data transformation to log.(x + 1). Log; river discharge volumes are

included. M1 = megalitres.

for other years. Growth for these three-month periods
varied from 4.0 mm for cohort 2 in 1980-1981 to 10.5
mm for cohort 3 in 1981-1982 (Figure 4). In addition to
varying seasonally, growth rates also varied with cohort

mean size. For example, the size of cohorts for all these
high-growth periods was small, with mean shell lengths
less than 5.6 mm. At other times, larger-sized cohorts
(>8.4 mm mean length) were present and their growth

Page 272

(A) (B)
1980 1981

012345 012345

012345

16
12

Number of individuals

012345 012345

|

012345 012345

The Veliger, Vol. 30, No. 3

(C) (D)
1982 1983

Feb.

012345 012345
| May

WIZB4SS 012345
Aug.

012345 012345
Nov.

=

012345 012345

Gametogenetic stages (0 - 5)
Figure 3

A-D. Temporal sequence of gametogenetic stages at site 7A from summer 1980 until spring 1983. The numbers
O to 5 on the abscissa refer to gametogenetic stages with 0 = resting or spent gonad, 1 = early active, 2 = late

active, 3 = ripe, 4 = partially spawned, and 5 = spent.

never exceeded 2.8 mm for any three-month period (Figure
4). Hence, the effect of season on growth rates was con-
founded by different sizes.

Growth rates also varied considerably among years. For
example, growth for the November-February period of
cohort 3 in 1981-1982 and cohort 5 in 1982-1983 was
10.5 mm and 4.8 mm respectively, even though the cohort
mean size was identical (Figure 4).

Distribution and Abundance in Space and Time

Differences in abundance among transects, depths, and
sediments, and with time, were often statistically signifi-
cant. However, the patterns of difference were not consis-
tent (ANOVA interaction terms significant) and, hence,
any ecological importance of the main factors was obscured
by complex interactions.

A. R. Jones et al., 1988

1980 1981

Number of individuals

i)
Gq) nm

rE

a |
= aa

Page 273

1982

Feb.

Aug.

: :
Nov.

20 2 20

1mm Pian intervals

Figure 4

A-P. Size-frequency histograms for each sampling time at site 7A. n = 200 for all samples except F, G, H, and
K where n = 46, 145, 110, and 140 respectively. The cohorts are numbered 1-6.

Along-estuary patterns: The occurrence of Notospisula
trigonella was restricted to the lower and middle reaches
of the estuary, 7.e., transects 1-9 inclusive. Although sig-
nificant differences in abundance among these transects
usually occurred (three-way ANOVA, Fpansec. = 243.2, P <
0.001; SNK tests), the pattern varied with both depth and
time (three-way ANOVA, all interaction terms signifi-
cant). The species was absent or rare from both deep and
shallow sites on transects 1 and 9. At deep sites, transects
2 and 3 were usually significantly richer than all other
transects, while no consistent along-estuary pattern of dif-
ference emerged from shallow sites (SNK tests, Figure 5).

Across-estuary patterns: Depth-related differences in
abundance occurred at all transects analyzed (three-way
ANOVA, Foeptn = 640.2, P < 0.001). However, the pattern
of difference varied with time (2.e., the richer site was
sometimes shallow and sometimes deep; ANOVA inter-
action terms significant, SNK tests) everywhere except at
transect 3. At transect 3, the deep site always yielded more
specimens than the shallow site although this depth-related
difference was confounded by sedimentary differences be-
tween the sites (Table 1).

At transect 6, sediments (but not water depth) varied
between the two sites (Table 1). Differences in abundance
between these sites were not significant during the first

five sampling times (two-way ANOVA, F,,,. = 4.1, P >
0.05; IB rreraction a Op P > 0.05).

Temporal patterns: For the long-term (7-yr) data, sig-
nificant seasonal and annual differences in abundance oc-
curred at both transect 2 (Foaon = 12.1, P < 0.001;
18.9 ye <0 001) kanditransect;/(Eee 5 Opel <
0.001; F,.., = 20.3, P < 0.001). However, at both transects
the seasonal patterns varied with both site and year and
the yearly patterns varied with both site and season (three-
way ANOVAs, second order interaction significant). De-
spite this significant interaction, patterns were relatively
cyclic at transect 7, where peaks often occurred in Novem-
ber and low densities in May or August (Figure 2). How-
ever, abundance varied irregularly at transect 2. Following
a major flood in March 1978, Notospisula trigonella was
absent from all sites sampled in May 1978 and relatively
rare in August 1978 (Figure 2).

Abundances at transects 2 and 7 were related to tem-
porally changing physicochemical factors in the following
ways. Spearman correlations between abundance and each
of salinity and one-month river discharge were significant
at sites 2.1, 7.1, and 7.2, but not at 2.2. Correlations with
temperature were significant only at sites 2.1 and 7.2 (Ta-
ble 2). Variation in these physicochemical factors never
accounted for more than 22% of variation in abundance.

Page 274

(log,(x+1))

Mean no. of individuals

Transect no. 1

Ee
0 Distance from river mouth (km) 30
Figure 5

Along-estuary distribution of mean number of individuals per
grab at shallow (©) and deep (@) sites for February 1977 (A)
and August 1977 (B). Standard errors are omitted for clarity but
varied from 0.0 to 0.5 (shallow, February), 0.0 to 0.5 (deep,
February), 0.0 to 0.2 (shallow, August), and 0.0 to 0.4 (deep,
August).

The Veliger, Vol. 30, No. 3

When the effects of two of the three physicochemical factors
were held constant by second order partial correlation, only
those correlations with salinity and temperature at site 7.2
were significant (Table 2).

DISCUSSION
Spawning and Recruitment

The appearance of a new cohort and the presence of
partly spawned animals in November of most years (Fig-
ures 3, 4) indicate that spawning usually starts just prior
to this month. This agrees with Hughes (personal com-
munication) who found that specimens from the Swan
Estuary in Western Australia first spawned in September-
October. These findings suggest that rising temperature
could be a spawning cue as found for other bivalve species
(SAsTRY, 1979). However, the variation in the onset and
duration of spawning among years, despite similar tem-
perature cycles, suggests that other factors could influence
spawning.

Salinity changes can also cause spawning in some bivalve
species (SASTRY, 1979) and spawning at low-flow (high-
salinity) times would promote retention of planktonic lar-
vae in the estuary. However, available evidence relating
spawning in Notospisula trigonella with salinity changes
are in conflict. For example, spawning occurred during
increasing salinities in Western Australia (Hughes, per-
sonal communication) and apparently during decreasing
salinities in Bramble Bay, Queensland (Stejskal, personal
communication). Furthermore, partly spawned individu-
als were observed during both low- and high-flow condi-
tions in the Hawkesbury Estuary. Hence, it appears that
any role of salinity change as a spawning cue is either
variable or else interacts with other factors.

Another feature of the life cycle of Notospisula trigonella
is the relationship between spawning and recruitment. Al-
though the length of the spawning period usually provided
the opportunity for extended recruitment from November
until February, only a single cohort appeared in most years

Table 2

Spearman (r,) and partial (7,) correlation coefficients between abundance of Notospisula trigonella and each physicochemical
variable at sites (2.1, 2.2, 7.1, and 7.2) with 7 yr of data available. Partial correlations are second order, 7.e., both other
physicochemical variables were controlled. *, **, *** = P < 0.05, 0.01, and 0.001 respectively, two-sided test.

2a
Physicochemical variable (n = 112)
Salinity Ts OB
is 0.12
River discharge is =0.25""
ins =O17/
Temperature , O25

r 0.04

Site
DD 7.1 VP
(n = 113) (n = 116) (n = 115)
—0.05 0.33*** 0.46***
0.15 0.12 0.23**
0.03 a OPS —0.36***
0.15 0.03 —0.17
0.04 0.18 OS
0.05 0.03 OBR

A. R. Jones et al., 1988

(Figure 4), always early in the spawning season. Any
settlement at other times did not yield specimens suffi-
ciently large to be sampled. STEJSKAL (1985) also found
recruitment in Bramble Bay, Queensland, restricted to
single cohorts. In the present study, several factors may
account for this pattern. For example, high river flows
after November in some years (Figure 2) may have washed
potential settlers downstream. Alternatively, the high den-
sities present after settlement of the first cohort may impede
further settlement through their suspension feeding on set-
tling individuals (WOoDIN, 1976). However, if this latter
mechanism does apply, it was insufficient to prevent the
settlement of two cohorts in 1982.

Growth

Growth rates varied seasonally, usually being highest
between November and February. At this time, most spec-
imens were small and, hence, the effects of season and size
on growth rate were confounded. The decline in growth
rate with size was probably caused by resources being
diverted from somatic to gonadal growth following the
onset of sexual maturity (CERRATO, 1980). However, other
factors associated with changing seasons may also have
influenced growth rates.

Growth rates also varied among years as shown by
comparisons between cohorts of similar mean size from
different years. From November 1981 to February 1982,
the growth rate was the highest recorded and more than
twice the rate for summer 1980-1981 and 1982-1983.
This high-growth period coincided with increased river
flows (but not of flood status) which may have enhanced
the food supply, hence accounting for the high level of
growth. Similarly, the growth rate for adults during spring
(August to November) of 1983, which experienced high
flows, was much greater than the growth rate of similar-
sized animals in 1980 when flows were low. However, the
relationship between growth and flow rate was non-mono-
tonic, as abundance was low or zero following the floods
of 1977 and 1978. Although few studies have related food
availability and bivalve growth, WILDISH & KRISTMANSON
(1985:237) showed that the growth of blue mussels “may
be controlled by tidal current speed through its effect on
seston supply.” Further, JOSEFSON (1982) found that food
supply rather than temperature affected the growth rate
of Abra alba.

Growth rates of Notospisula trigonella also appear to
vary with geographical location. For example, the
Hawkesbury cohort 3 (Figures 4H-K) reached its max-
imum size (19 mm mean shell length) in nine months and
may have persisted for only 12-15 months. By contrast,
individuals of N. trigonella from Bramble Bay, Queens-
land, were only 14-16 mm long at an estimated age of 20-
24 months (Stejskal, personal communication). Alterna-
tively, the population at Bramble Bay may have grown
more slowly because it was intertidal (and hence had less
feeding time) rather than some geographical factor, or else
because age estimates might have been in error.

Page 275

Because of the limitations imposed by the low temporal
resolution in sampling, the above life-history interpreta-
tions have provisional status only.

Distribution and Abundance

Spatial differences in abundance were not only usually
statistically significant but also inconsistent. Such vari-
ability appears common both for Notospisula trigonella else-
where (STEJSKAL, 1985) and for other bivalve species
(O’FOIGHIL et al., 1984; GiBBs, 1984). Although these
inconsistent patterns make it difficult to suggest factors
controlling abundance, available evidence suggests the up-
stream limit of N. trigonella may be influenced by salinity.
Hughes (personal communication) found high mortality
in laboratory populations held in salinities below 5%o, and
both this study and that of PooRE (1982) in the Gippsland
Lakes failed to find this species below 10%o in depths and
sediment grades similar to populated sites of higher salin-
ity.

Although no consistent downstream distributional limit
was observed in the present study, Notospisula trigonella
was absent or rare from transect 1 and also from the high-
salinity sites near the mouth of the Gippsland Lakes
(Poor, 1982). Furthermore, abundance in large marine
bays can be enhanced near freshwater inputs (POORE &
RAINER, 1974; STEJSKAL, 1985). These results suggest that
marine salinities or some associated factor (see, e.g., BOESCH,
1977) inhibit N. trigonella.

Significant across-estuary differences in abundance were
sometimes associated with both depth and sediment grade.
These patterns resemble those of other mactrid bivalve
species (HOLLAND, 1985). However, neither depth nor
sediment grade was useful for predicting abundance be-
cause the nature of the relationship varied with time, lo-
cation, or both. Furthermore, at transect 6 where sediment
changes were not confounded with depth, significant dif-
ferences in abundance did not occur. These results suggest
that sediment specificity is low in this species. Other studies
have found Notospisula trigonella to occupy sediments rang-
ing from mud (PooRE & KUDENOv, 1978) to sand
(MACPHERSON & GABRIEL, 1962; Hughes, personal com-
munication). However, experimental work by Jones (per-
sonal communication) found that silt and fine sand at-
tracted more specimens than coarse sand (which did not
characterize any Hawkesbury site) where burrowing was
difficult. Of course, factors such as hydrodynamic forces
are confounded with water depth and sediment grade and
may influence adult abundance through their effect on
larval distribution or food supply.

Temporal Patterns

While temporal differences in abundance were often
highly significant, the patterns of difference were very
variable. For example, seasonal differences were not al-
ways repeatable over years. Some of this variation can be

Page 276

explained by the occurrence of a major flood in March
1978 and a minor flood in March 1977 after which No-
tospisula trigonella was uniquely absent and rare respec-
tively. Hence, the seasonal patterns of abundance were
altered for these years.

Other estuarine invertebrate species also show substan-
tial temporal variability (BOESCH e¢ al., 1976a; HOLLAND,
1985). One of these is the mactrid bivalve Mulinia lateralis
which exhibits high fecundity, rapid growth, and early
maturity (BOESCH et al., 1976a). Notospisula trigonella shares
some of these traits, which probably promote survival in
a variable and disturbance-prone environment (GRASSLE
& SANDERS, 1973).

In contrast, another estuarine mactrid bivalve, Rangia
cuneata, has a life history that differs from the above species
by having long life (at least 8 yr) and by being persistently
present in samples taken between 1969 and 1975 (BOESCH
et al., 1976a). Temporal variability in abundance was also
comparatively low. Consequently, attempts to generalize
about estuarine life-history strategies, even among confa-
milial species, will fail. However, a partial explanation of
these differing strategies arises from the following. Estu-
aries are far from uniform habitats, and species in different
salinity zones often differ in their response to disturbance
(BOESCH et al., 1976b; Jones, in preparation). Mulinia
lateralis and Notospisula trigonella both inhabit salinities
exceeding 10%o where flood-induced salinity depression,
and hence the magnitude of disturbance, would be greater
than for R. cuneata, which lives in salinities lower than
10%o. Unlike the other two mactrids, R. cuneata can survive
severe flooding with the probable consequence of longer
life and increased buffering of temporal fluctuations.

Although the decreased abundance of Notospisula tri-
gonella associated with floods suggests that greatly de-
creased salinity lowers abundance, the effect of salinity is
confounded with the sediment changes that accompany
floods. Sediment erosion and deposition and turbidity can
kill other bivalve species (PERKINS, 1974; PETERSON, 1985).
Being a surface-dwelling suspension feeder with short si-
phons, N. trigonella would probably be particularly sus-
ceptible to these sediment changes, especially as Jones
(personal communication) found sediment disturbance to
affect significantly the abundance of this species.

Although some short-term changes can be explained by
the effects of floods, factors such as salinity, river discharge,
and temperature never explained more than 22% of the
long-term variation (Table 2), a similar result to that
obtained for Mulinia lateralis in the Chesapeake Bay
(HOLLAND, 1985). Furthermore, most of the partial cor-
relations concerning Notospisula trigonella were not sig-
nificant. This high degree of unexplained variability is
typical of the zoobenthos of the Hawkesbury Estuary,
where rainfall is itself temporally unpredictable (Jones et
al., in preparation).

ACKNOWLEDGMENTS

Weare grateful to malacologists at the Australian Museum
(Dr. W. F. Ponder, Dr. W. B. Rudman, Mr. I. W. Loch,

The Veliger, Vol. 30, No. 3

and Mr. P. Colman) and Dr. I. Stejskal and Professor D.
T. Anderson for advice concerning taxonomy, biology, and
histological interpretations. Dr. G. H. Pyke, Dr. Rudman,
Mr. Loch, and two anonymous referees also made con-
structive comments on the manuscript. We also thank our
boat skipper Mr. John Reed for his seamanship, Mr. R.
Bateman and Mr. F. Byers for analyzing sediments, and
the Coastal Council of N.S.W., the State Pollution Control
Commission of N.S.W., and the Australian Museum Trust
for financial support. The Metropolitan Water Sewerage
and Drainage Board and the Water Resources Commis-
sion provided river discharge data. Above all, we are in-
debted to Mss. Robin Marsh and Charlotte Watson-Rus-
sell for their contributions to field and laboratory aspects
of this project.

LITERATURE CITED

BosscH, D. F. 1977. A new look at the zonation of benthos
along the estuarine gradient. Pp. 245-266. Jn: B. C. Coull
(ed.), Ecology of marine benthos. Univ. South Carolina Press:
Columbia.

Bosscu, D. F., R. J. Diaz & R. W. VIRNSTEIN. 1976b. Effects
of tropical storm Agnes on soft-bottom macrobenthic com-
munities of the James and York Estuaries and the Lower
Chesapeake Bay. Chesapeake Sci. 17:246-259.

Bosscu, D. F., M. L. Wass & R. W. VIRNSTEIN. 1976a. The
dynamics of estuarine benthic communities. Pp. 177-196.
In: M. Wiley (ed.), Estuarine processes. Vol. 1. Uses, stress-
es, and adaptation to the estuary. Academic Press: New York.

BRALEY, R. D. 1984. Mariculture potential of introduced oys-
ters Saccostrea cucullata tuberculata and Crassostrea echinata
and a histological study of the reproduction of C. echinata.
Aust. Jour. Mar. Freshwater Res. 35:129-141.

CARLETON, H.M. 1957. Histological technique. 3rd ed. Chap-
ter VII, pp. 93-100. Oxford University Press: London.

CassiE, R. M. 1954. Some uses of probability paper in the
analysis of size frequency distributions. Aust. Jour. Mar.
Freshwater Res. 5:513-522.

CERRATO, R. M. 1980. Demographic analysis of bivalve pop-
ulations. Pp. 417-465. In: D. C. Rhoads & R. A. Lutz (eds.),
Skeletal growth of aquatic organisms: biological records of
environmental change. Plenum Press: New York.

CHALMER, P. N., E. P. HODGKIN & G. W. KENDRICK. 1976.
Benthic faunal changes in a seasonal estuary of South-west-
ern Australia. Rec. West. Aust. Mus. 4(4):383-410.

Foik, R. L. 1974. Petrology of sedimentary rocks. Hemphill:
Austin. 182 pp.

Gipss, P. E.. 1984. The population cycle of the bivalve Abra
tenuis and its mode of reproduction. Jour. Mar. Biol. Assoc.
U.K. 64:791-800.

GRASSLE, J. F. & H. L. SANDERS. 1973. Life histories and the
role of disturbance. Deep-Sea Res. 20:643-659.

GREEN, R. H. 1968. Mortality and stability in a low diversity
subtropical intertidal community. Ecology 49:848-854.
HOLLAND, A. F. 1985. Long-term variation of macrobenthos
in a mesohaline region of Chesapeake Bay. Estuaries 8:93-

113.

JosEFson, A. B. 1982. Regulation of population size growth
and production of a deposit-feeding bivalve: a long-term field
study of three deep-water populations off the Swedish coast.
Jour. Exp. Mar. Biol. Ecol. 59:125-150.

MacPHERSON, J. H. & C. J. GABRIEL. 1962. Marine molluscs
of Victoria. Melbourne University Press: Melbourne. 475

PP-

A. R. Jones et al., 1988

Page 277

McLacuian, A. & T. Erasmus. 1974. Temperature toler-
ances and osmoregulation in some estuarine bivalves. Zool.
Africana 9(1):1-13.

O’FoIGHIL, D., D. McGRraTH, M. E. CONNEELY, B. F. KEEGAN
& M. CosTELLoeE. 1984. Population dynamics and repro-
duction of Mysella bidentata (Bivalvia: Galeommatacea) in
Galway Bay, Irish west coast. Mar. Biol. 81:283-291.

PERKINS, E. J. 1974. The biology of estuaries and coastal
waters. Academic Press: London. 678 pp.

PETERSON, C. H. 1985. Patterns of lagoonal bivalve mortality
after heavy sedimentation and their paleoecological signifi-
cance. Paleobiology 11:139-153.

Poors, G. C. B. 1982. Benthic communities of the Gippsland
Lakes, Victoria. Aust. Jour. Mar. Freshwater Res. 33:901-
915.

Poore, G. C. B. & J. D. KUDENOv. 1978. Benthos of the Port
of Melbourne: the Yarra River and Hobson’s Bay, Victoria.
Aust. Jour. Mar. Freshwater Res. 29:141-1506.

Poore, G. C. B. & S. RAINER. 1974. Distribution and abun-
dance of soft-bottom molluscs in Port Phillip Bay, Victoria,
Australia. Aust. Jour. Mar. Freshwater Res. 25:371-411.

RAINER, S. F. & R. C. FITZHARDINGE. 1981. Benthic com-
munities in an estuary with periodic deoxygenation. Aust.
Jour. Mar. Freshwater Res. 32:227-243.

Roperts, D. 1984. A comparative study of Lasaea australis,
Vulsella spongiarum, Pinna bicolor and Donacilla cuneata
(Mollusca; Bivalvia) from Princess Royal Harbour, Western
Australia. Jour. Moll. Stud. 50:129-136.

RoBINSON, K. & P. Gipps. 1982. A field guide to the common
shelled molluscs of New South Wales estuaries. Coast and
Wetlands Society: Sydney. 56 pp.

Ropes, J. W. 1968. Reproductive cycle of the surf clam, Spisula
solidissima, in offshore New Jersey. Biol. Bull. 135:349-365.

Sastry, A. N. 1979. Pelecypoda (excluding Ostreidae). Chap-
ter 5. In: A. C. Giese & J. S. Pearse (eds.), Reproduction
of marine invertebrates. Vol. V. Molluscs: Pelecypods and
lesser classes. Academic Press: New York.

STEJSKAL, I. 1985. The spatial and temporal patterns of the
macrofauna of a subtropical muddy sandflat in southeast
Queensland, Australia. Ph.D. Thesis, University of Queens-
land, Brisbane.

STEPHENSON, W., S. D. Cook & Y. I. RAPHAEL. 1977. The
effect of a major flood on the macrobenthos of Bramble Bay,
Queensland. Mem. Queensl. Mus. 18:95-119.

WEINBERG, J.R. 1985. Factors regulating population dynamics
of the marine bivalve Gemma gemma: intraspecific compe-
tition and salinity. Mar. Biol. 86:173~-182.

WILpIsH, D. J. & D. D. KRISTMANSON. 1985. Control of
suspension feeding bivalve production by current speed. Hel-
golander wiss. Meeresunters 30:445-454.

WILSON, B. R. 1969. Survival and reproduction of the mussel
Xenostrobus securis (Lamarck) (Mollusca; Bivalvia; Mytili-
dae) in a Western Australian estuary. Pt. II: Reproduction,
growth and longevity. Jour. Natur. Hist. 3:93-120.

WILSON, B. R. & G. W. KENDRICK. 1968. The recent ap-
pearance of Notospisula parva (Lamarck) (Mollusca; Bival-
via; Mactridae) in the Swan Estuary. Jour. Malacol. Soc.
Aust. 1:25-31.

Woop, S. A. 1976. Adult-larval interactions in dense faunal
assemblages: patterns of abundance. Jour. Mar. Res. 34:25-
41.

The Veliger 30(3):278-290 (January 4, 1988)

THE VELIGER
© CMS, Inc., 1988

Reproduction in a Brackish-Water Mytilid:

Gametogenesis and Embryonic Development

by

R. T. F. BERNARD,' B. R. DAVIES,? anp A. N. HODGSON!

' Department of Zoology and Entomology, Rhodes University, Grahamstown 6140, South Africa
* Freshwater Research Unit, Department of Zoology, University of Cape Town 7700, South Africa

Abstract.

The fine structure of gametogenesis, ultrastructure of the gametes, and embryonic devel-

opment at a salinity of 9%o and at three temperatures (15, 20, and 24°C) of the brackish-water mussel
Brachidontes virgiliae (Barnard) are described. The spermatozoon is similar to that found in other
Pteriomorphia, with a mid-piece of five or six mitochondria, a round electron-dense nucleus, and a
hollow conical acrosome. Implications of spermatozoon structure in determining the taxonomic position
of this species are discussed. Three stages of oogenesis were recognized: previtellogenic, and early and
late vitellogenic. Cortical granules appear to be the source of the vitelline membrane material. The
embryonic development of B. virgiliae is rapid at 24°C, with spat formation within 24 h of fertilization.
Development slows by a factor of 1.5 at 20°C and 2.3 at 15°C. About 18% of developing ova fail to
reach the spat stage at 20 and 24°C, increasing to 34% at 15°C. The embryonic development of the
animal is discussed in the light of its ecology in southern Cape estuaries and coastal lakes.

INTRODUCTION

Brachidontes virgiliae (Barnard, 1964) is a mytilid bivalve
mollusk found in South African waters from the Great
Brak River to Mozambique (BARNARD, 1964). The mussel
was first identified and named Musculus virgiliae by
BARNARD in 1964, the name being confirmed by DAVIES
(1980). More recently KILBURN & RIPPEY (1982) claim
that the animal belongs to the genus Brachidontes, although
they point out that this is by no means certain. Despite
the uncertairity, however, we have elected to use the more
recent classification and name.

Apart from descriptive work, there is limited informa-
tion on the biology and ecology of the species. A few un-
published works deal with its distribution, feeding, repro-
duction, and spatfall (MCLAREN, 1977; PLUMSTEAD, 1976;
SHARP, 1977; COETZEE, 1978). DAviEs (1980) noted that
Brachidontes virgiliae inhabits the upper reaches of estu-
aries, favoring low, fluctuating salinities (<15%o) in areas
where the substratum is relatively free of silt. Although a
small bivalve (maximum shell length 30 mm), B. virgiliae
is an extremely important component of the invertebrate
standing stocks of many coastal lakes along the southern
and eastern seaboard of South Africa (BOLTT, 1973; AL-
LANSON, 1981; DAviIEs, 1982, 1984). A recent decline in
standing stocks of the littoral macrophyte Potamogeton pec-
tinatus Linnaeus in these coastal systems and a concomitant

collapse of the B. virgiliae populations has had profound
effects upon the food chains, with particularly severe con-
sequences for the ichthyofauna (WHITFIELD, 1982, 1984).
Clearly further ecological studies on this bivalve are called
for, especially with regard to its association with P. pec-
tinatus in these systems.

In this study we describe, using microscopic techniques,
the fine structure of gametogenesis, the structure of the
spermatozoon (which may aid the classification of this
species), and the embryonic development of the organism.

MATERIALS anpD METHODS

Gametogenesis

Specimens were collected during January and February
1984 from boulders at the head of the Kowie estuary
(33°36'S, 26°54’E; Figure 1). Portions of testes and ovaries,
which are found mainly in the mantle lobes, were excised
from the animals and prepared for electron microscopy.
Tissues were fixed in 2.5% phosphate buffered (pH 7.2)
glutaraldehyde at 4°C and left overnight. After washing
with phosphate buffer (pH 7.2) small pieces of tissue were
post-fixed in 1.0% osmium tetroxide for 90 min, dehy-
drated, and embedded in Taab 812 resin via propylene
oxide. Thin sections were cut with a glass knife, stained
with uranyl acetate (30 min) and lead citrate (3 min), and
examined with a JEOL 100 CXII microscope.

Reet kee becnandicial slo 8s

In Vitro Embryonic Development

In vitro fertilization experiments were carried out dur-
ing the summer of 1978. Viable eggs and spermatozoa
were obtained from animals kept in continuous culture
and ‘“‘wild” stocks from Swartvlei (34°0'S, 22°46’E) and
the head of the Kowie estuary (Figure 1).

Swartvlei populations of Brachidontes virgiliae were nor-
mally sexually active at shell lengths from 5 to 6 mm, at
which size the gonads could clearly be seen through the
thin shell when viewed under transmitted light. The go-
nads within the mantle wall are typically branched struc-
tures: female, brown to russet in color (the species is dioe-
cious), and male gonads, creamy white. Swartvlei stocks
maintained in continuous culture systems at a salinity of
4%o provided gametes at shell lengths between 6 and 10
mm, while those maintained at 9%o provided viable gametes
at shell lengths of 7 mm and larger. Stocks from the Kowie
estuary provided viable gametes at shell lengths greater
than 10 mm and showed no signs of sexual activity below
this size. Because of the thickness of the shell, the sex and
state of gonad development of these individuals could only
be determined by opening the shell valves. Specimens from
the estuarine population were frequently used for in vitro
fertilization experiments, but shell lengths between 15 and
27 mm gave the most consistent results in terms of suc-
cessful embryonic development. Animals from either source,
which were less than 4.5 mm shell length, were invariably
of indeterminate sex, although gonad development was
visible in a few cases (mainly Swartvlei “wild” stocks).

In vitro fertilization experiments and observations of
embryonic development were carried out in petri dishes
containing filtered water maintained at a salinity of 9%o
and at temperatures of 15 + 2, 20 + 2, and 24 + 2°C.
Gametes were obtained by removing the right valve and
rupturing the exposed mantle with a fine needle. Eggs and
spermatozoa released in this way were rapidly caught up
by the ciliary currents of the gills and carried along the
feeding grooves to the labial palps. Here they collected and
were either periodically gathered by the tip of the foot and
pushed ventrally from the cavity or were picked up by
currents along the inner mantle wall and discharged through
the posterodorsal exhalant siphon. Gametes were trans-
ferred to cavity slides or glass wells using micropipettes,
mixed, and subsequently monitored using a Wild stereo-
microscope. Development was photographed using an
Olympus Vanox automatic exposure system.

RESULTS

Spermatogenesis

Most stages of spermatogenesis may be observed
throughout the year. Early spermatogonia lie close to the
haemocoelic space that surrounds each germinal follicle
and are characterized by a large spherical or ellipsoidal
nucleus (4 x 5 wm) with a prominent electron-dense nu-
cleolus (0.7 wm diameter) (Figure 2). The nucleus contains

Page 279

25 30E
Figure |

Map showing the positions of Swartvlei and Kowie estuaries on
the coast of southern Africa, from which specimens of Brachidontes
virgiliae were collected for studies of gametogenesis and embryonic
development.

small clumps of electron-dense chromatin which are often
associated with the inner nuclear membrane. The cyto-
plasm contains numerous small mitochondria (0.3 wm di-
ameter), free ribosomes, and rough endoplasmic reticulum.
Late spermatogonia have a smaller nucleus (ca. 3 um di-
ameter) with a more granular electron-dense nucleoplasm
(Figure 2).

Two stages of spermatocyte development, presumed to
be primary and secondary, can be found in the walls of
the germinal follicle of some specimens. The nucleus of
the spermatocyte is similar in size and shape to that of the
late spermatogonium; however, the nucleolus is no longer
prominent and the chromatin is in the form of a patchwork
(Figure 2). The cytoplasm contains a similar complement
of organelles to the spermatogonia, as well as Golgi bodies
and a few dense, osmiophilic granules—the proacrosomal
vesicles (Figure 2)—which are formed by the Golgi bodies.
Although similar in size and organelle complement to the
primary spermatocyte, the secondary spermatocyte is char-
acterized by less osmiophilic chromatin.

In the early stages of spermatid development the nucleus
is spherical and occupies the center of the cell (Figure 3).
The cytoplasm contains numerous mitochondria, rough
endoplasmic reticulum, Golgi bodies, and proacrosomal
vesicles. Intercellular bridges connect the spermatids. As
they mature, spermatids are displaced towards the center
of the germinal follicle, cytoplasm is lost by sloughing
(although cells remain joined by bridges), and the nuclear
contents begin to condense (Figure 3). Proacrosomal ves-
icles migrate to the presumptive anterior of the cell where
they coalesce to form a single electron-dense vesicle (Figure

Page 280

4), while mitochondria become less numerous but increase
in size.

As development progresses, the mitochondria come to
occupy the end of the cell opposite the acrosome, forming

The Veliger, Vol. 30, No. 3

Explanation of Figures 2 to 4

Figure 2. Section through a germinal follicle wall in the testis of
Brachidontes virgiliae. ESG, early spermatogonium; H, haemo-
coelic space; LSG, late spermatogonium; m, mitochondrion; no,
nucleolus; pav, proacrosomal vesicles; SC, spermatocyte. Scale
bar = 2 um.

Figure 3. Portion of a germinal follicle showing spermatids (ST)
and a mature spermatozoon (S). Note the intercellular bridge
(arrow) linking two spermatids. Scale bar = 2 wm.

Figure 4. Longitudinal section through the middle of a late sper-
matid showing structure of the acrosome (A) after the proacro-
somal vesicles have coalesced. Note the excess cytoplasm (cy) still
surrounding the nucleus and the proximity of the mitochondria
(m) to the nucleus. Scale bar = 1 um.

the sperm mid-piece, and there is a steady loss of cytoplasm
by sloughing, a decrease in nuclear size, and a condensation
of nuclear material. The acrosomal vesicle assumes an oval
shape with the short axis in the anteroposterior plane of

Revere Bernardiciial 988 Page 281

Figure 5

Longitudinal (A) and transverse (B-E) sections through a spermatozoon. B and C are sections through the acrosome;
D through the nucleus, and E, the mid-piece. Key: A, acrosome; ed, electron-dense region of acrosome; el, electron-
lucent region of acrosome; gly, glycogen; N, nucleus; sm, subacrosomal material; T, tail. Scale bar = 1 um.

the spermatid (Figure 4). This is followed by invagination and tail, occupy a more central position within the follicle.
of the adnuclear surface and elongation to form the char- The head is a 1.8-um long structure with a round to oval
acteristic hollow conical-shaped acrosome (Figure 5). electron-dense nucleus (ca. 1.5 wm diameter) with a char-

Mature spermatozoa, each comprising head, mid-piece, acteristic anterior fossa (Figure 5A) and an acrosome 0.5

The Veliger, Vol. 30, No. 3

Page 282

R. T. F. Bernard et al., 1988

um long. The hollow, conical acrosome has a uniformly
thick wall and contains both an outer electron-dense and
inner electron-lucent substance (Figure 5A). Beneath the
acrosome is subacrosomal material that has a granular
appearance (Figures 5A, C).

The mid-piece contains six (rarely five) spherical mi-
tochondria (Figure 5E) which lie tightly against the nu-
cleus. Glycogen granules lie between the mitochondria while
in the center of the ring are the proximal and distal cen-
trioles (Figures 5A, E). The tail, which originates from
the distal centriole, has the typical 9+2 arrangement of
microtubules (Figure 5A).

Oocyte Maturation

Three stages of oocyte maturation (previtellogenic, early
vitellogenic, and late vitellogenic) can be recognized in the
ovary of Brachidontes virgiliae. The previtellogenic oocyte
is about 17 wm in diameter with a large (9 wm diameter)
nucleus and a prominent nucleolus (Figure 6). The cell
membrane has no microvilli and the vitelline membrane
has not yet been formed. The cytoplasm is highly granular
and contains numerous spherical and rod-shaped mito-
chondria, many of which are in a perinuclear position
(Figure 6), some strands of rough endoplasmic reticulum,
and a few cortical granules. The previtellogenic oocyte is
surrounded by several follicular cells which are charac-
teristically irregular in shape with large nuclei (Figure 6).
The cytoplasm of the follicular cells is not as electron-
dense as that of the oocyte and contains many glycogen
granules, some mitochondria, and rough endoplasmic re-
ticulum (Figures 6-8).

During the two vitellogenic stages there is production
of lipid and protein yolk bodies and probably the continued
production of cortical granules. Lipid yolk bodies, which
are commonly found in association with mitochondria
(Figure 8), are spherical and of variable size. They are
not membrane bound, occur in clumps, and are relatively
electron-lucent (Figures 7-9). Protein yolk bodies occur
in two forms: in one, the contents appear to comprise
numerous small vesicles, with areas of variable electron
density (Figure 9, inset), while in the other, the contents
are uniformly electron-dense (Figure 7). Both types of
protein yolk body are spherical and membrane bound (Fig-

Explanation

Figure 6. Section through a previtellogenic oocyte showing its
peripheral position in the gonad. Note that the oocyte, with its
nucleus (N) and prominent nucleolus is surrounded by follicular
cells (fc). cg, cortical granule; m, mitochondria; ME, mantle
epithelium. Scale bar = 5 um.

Figure 7. Section through part of a vitellogenic oocyte showing
lipid yolk bodies (ly), protein yolk bodies (py), and cortical gran-
ules (cg). Note also the structure of the vitelline membrane (vm)

Page 283

ures 7, 9). The cortical granules are of variable shape
(often ovoid), occur singly, are membrane bound, and are
of intermediate electron density (Figure 7).

During early vitellogenesis the cell membrane develops
microvilli and the vitelline membrane is laid down (Figure
10). Associated with this deposition of the vitelline mem-
brane is an arrangement of some of the cortical granules
so as to be in contact with the oocyte cell membrane (Figure
10). Early vitellogenesis is further characterized by an
increase in nuclear diameter to about 25 um, with the
nucleus becoming increasingly irregular in shape and the
nuclear membrane more porous (Figures 10, 11). In ad-
dition to protein and lipid yolk bodies and cortical granules,
the cytoplasm of the early vitellogenic oocyte contains nu-
merous mitochondria, complex arrays of rough endoplas-
mic reticulum, and few Golgi bodies with associated ves-
icles (Figures 8, 9). In the early vitellogenic oocyte the
cortical granules, protein, and lipid yolk bodies occur in
the ratio 1:2:3. In the cytoplasm of the late vitellogenic or
full-size oocyte (Figure 12), the cortical granules, protein,
and lipid yolk bodies are abundant and occur in the ratio
1:4:5. At this stage the vitelline membrane is fully formed,
and there has been no change in the complement of oocyte
organelles. The follicular cells of the full-size oocyte are
restricted to those parts of the oocyte that are in proximity
to the germinal epithelium of the gonad.

In Vitro Embryonic Development

Development at 9% and 24 + 2°C: Eggs are spherical,
granular and russet-brown in color, with a mean diameter
of 38.3 um (SE = +3.6 um, n = 300) (Figure 13A).
Embryonic development is rapid and the results for 23
separate in vitro fertilization experiments carried out at
9%o and 24 + 2°C are summarized in Table 1.

Within 5 min of mixing gametes, polar body extrusion
is evident (Figure 13A; Table 1). The first division to
produce a micro- and a megamere takes place within 25
min of fertilization (Figure 13A) and is followed by a
second division within 45 min. Normally this takes place
by division of the megamere (Figure 13A), but occasionally
micromere divisions can be observed. The 8-cell stage is
reached 115 min after fertilization (Table 1) and is fol-
lowed by very rapid dexiotropic cleavage to form a blastula

of Figures 6 to 9

and the glycogen in the follicular cell (fc). rer, rough endoplasmic
reticulum. Scale bar = 1 pm.

Figure 8. Part of an early vitellogenic oocyte showing parallel
arrays of rough endoplasmic reticulum (rer) and the close as-
sociation of mitochondria (m) and lipid yolk bodies (ly). fc, follicle
cell; G, Golgi body; N, nucleus. Scale bar = 1 um.

Figure 9. Higher magnification of Golgi body and associated

vesicles. Inset: protein yolk body from early vitellogenic oocyte.
Scale for figure and inset the same, bar = 0.5 um.

Page 284 The Veliger, Vol. 30, No. 3

R. T. F. Bernard e¢ al., 1988

(Figure 13B) some 4 h post-fertilization. Gastrulation
(epibolic) occurs between 4 and 5 h (Figure 13C) and the
morula begins to perform spiral swimming movements, as
short ectodermal cirri begin to develop (Figure 14A).

Between 5 and 10h after fertilization, the morula under-
goes rapid organ differentiation, commencing with the de-
velopment of velar cirri and velar lobes (Table 1), and by
10 h obvious veliger larvae (Figure 14B) are actively swim-
ming, with more directed movements than the simple spiral
swimming of earlier stages. After 20 h, embryonic devel-
opment has progressed to the “early spat” stage, with the
formation of the larval shell and regression of the velar
lobes (Figure 14C). At this time, larvae respond to dis-
turbance by cessation of swimming and sinking through
the water column. A few hours later (ca. 24 h post-fertil-
ization), the characteristic bilaterally flattened spat is ob-
vious (Figure 14D), with a thickened shell and a pro-
nounced hinge ligament. Adductor muscles are functional
at this stage and, as before, the spat exhibit “avoidance”
reactions to disturbance by closing the valves, cessation of
swimming, and sinking to the bottom of the culture vessel.
The rudimentary foot is ciliated and much of the swimming
movements of spat are directed by this structure. The de-
veloping gut is visible through the transparent shell.

Additional observations indicate that spat remain active
for at least a further 48 h (up to 72 h post-fertilization)
after which they tend to reduce swimming activities and
settle on the bottom of the culture vessel. Approximately
18% of fertilized ova fail to develop to the spat stage and
of these, most fail to reach the 8-cell stage, while the
remainder suffer deformity during transition from blastula
to the early veliger larva.

Development at 9%o and 15 + 2 or 20 + 2°C: In vitro
embryonic development experiments at a salinity of 9%o
and at temperatures of 15 + 2 and 20 + 2°C were carried
out during January 1979. The averaged results of four
experiments at 15°C and seven at 20°C are listed in Table
2. Briefly, temperature reduction to 15°C slows develop-
ment by a factor of 2.3 in terms of the time taken to reach
the spat stage (up to 55 h post-fertilization). More im-
portant, perhaps, is the proportion of fertilized ova that
fail to reach the spat stage—approximately 34%. In this
case, most developmental failures occur in the very early
stages (first and second cleavage). Embryonic development
at 20°C slows by 12 h compared to that at 24°C (Table
2), while the failure rate is similar (ca. 16%).

At both 15 and 20°C, spat remain active for over 72 h

Page 285

post-fertilization and show no sign of settling. The lon-
gevity of spat at these temperatures is, however, unknown
because of culture maintenance problems. Spat usually
begin to show signs of osmotic stress after 70 h even after
careful attempts to reduce water loss from culture vessels.

DISCUSSION

The structure of the spermatozoon of Brachidontes virgiliae
is similar to that described for other bivalves of the subclass
Pteriomorphia (POPHAM, 1979). The spermatozoa of such
bivalves have a mid-piece of 4-6 mitochondria and a head
comprising a round electron-dense nucleus capped by a
conical acrosome. It has been suggested that, when eval-
uated correctly, the ultrastructure of spermatozoa can be
used for taxonomic purposes or as an aid to the identifi-
cation of invertebrates (POPHAM, 1979; BACCETTI, 1979;
ADIYODI & ADIYODI, 1983; FRANZEN, 1983). Recent work
on two closely related species of Mytilus, M. edulis (Lin-
naeus) and M. galloprovincialis Lamarck, has shown this
to be so (HODGSON & BERNARD, 1986), for although these
mussels are difficult to separate on shell characteristics,
they are easily separated using spermatozoon morphology.

In the case of Brachidontes virgiliae, identification is still
in doubt (KILBURN & RIpPPEY, 1982); it was originally
classified as Musculus virgiliae by BARNARD (1964). In an
attempt to shed some light on its position, we have com-
pared the spermatozoon of B. virgiliae with that of M.
discors, which was described by FRANZEN (1983). Figure
15 shows that the two spermatozoa are very different,
suggesting that the two bivalves do not belong to the same
genus. The difference, however, may be more closely linked
to the mode of fertilization employed by each species.
FRANZEN (1983), for example, has noted that some inver-
tebrates having a modified reproductive biology have an
elongate nucleus. Musculus discors has direct development,
with simple brood protection (THORSON, 1935). Brachi-
dontes virgiliae, on the other hand, employs external fer-
tilization, and like all other bivalves with external fertil-
ization, it has a primitive spermatozoon (FRANZEN, 1983).
Clearly a comparative investigation of other species of
Brachidontes and Musculus, supported by electrophoresis,
is required before the problem of the correct identification
of B. virgiliae can be solved.

The observations presented here on spermatogenesis
mirror the findings of LONGO & DORNFELD (1967) for
Mytilus edulis and BERNARD & HODGSON (1985) for Perna
perna (Linnaeus). The greatest changes in cell morphology

Explanation of Figures 10 to 12

Figure 10. Section through an oocyte at the early vitellogenic
stage showing the enlarged nucleus (N) with irregular border.
Note the alignment of the cortical granules (arrows) next to the
vitelline membrane (vm). Scale bar = 1 um.

Figure 11. Section through an oocyte at the vitellogenic stage

showing the irregular nuclear membrane, with numerous nuclear
pores (np). Scale bar = 0.5 um.

Figure 12. Section through part of the full-size oocyte showing
the accumulation of lipid (ly) and protein (py) yolk bodies in the
ooplasm. Scale bar = 2 um.

Page 286 The Veliger, Vol. 30, No. 3

Figure 13

Photomicrographs of embryonic development of Brachidontes virgiliae at 24°C and 9%o. A. The newly fertilized egg
(1) has a granular cytoplasm and vitelline membrane. Five minutes after fertilization the polar body (2) has been
extruded, and first cleavage to produce distinct micro- and megamere (3) occurred within 30 min. (4) shows the
first megamere about to cleave, and (5) a 4-cell embryo. Scale bar = 25 um. B. Early blastula, 4 h post-fertilization.
Scale bar = 10 um. Early gastrula, approximately 4.5 h after fertilization. Scale bar = 5 um.

R. T. F. Bernard et al., 1988

occur at the spermatid stage, with nuclear chromatin con-
densation, mitochondrial fusion to form the mid-piece, and
acrosome formation.

Two significant processes occur during oocyte matu-
ration: the production and accumulation of yolk, and the
deposition of the vitelline membrane. It is generally ac-
cepted that in mollusks, lipid yolk bodies are formed in
association with mitochondria (BEAMS & SEKHON, 1966;
NoRREVANG, 1968; DE JONG-BRINK et al., 1983) and the
close physical association between lipid yolk bodies and
mitochondria in Brachidontes virgiliae supports this view.
Several sources have been proposed for the protein yolk
bodies (see NORREVANG, 1968, for review). HUMPHREYS
(1962) has described bodies intermediate between mito-
chondria and protein yolk platelets in the oocytes of Mytilus
edulis; such structures were not, however, seen in B. vwi7-
giliae. BEAMS & SEKHON (1966), ANDERSON (1969), and
TAYLOR & ANDERSON (1969) have suggested that rough
endoplasmic reticulum produces a precursor that is mod-
ified by the Golgi bodies and released as small vesicles,
which later unite to form the definitive protein yolk body.
Based on the abundance of rough endoplasmic reticulum,
the presence of Golgi bodies, and the appearance of the
two types of protein yolk body, we would suggest that these
bodies in B. virgiliae are formed via a similar route, and
further, that the protein yolk body in which small vesicles
can be seen, is an intermediate stage.

The vitelline membrane, which is laid down in early
vitellogenesis, is a product of the oocyte (DE JONG-BRINK
et al., 1983), and in Mytilus edulis, the cortical granules
may be the source of this material (HUMPHREYS, 1967).
The arrangement of cortical granules, in contact with or
very close to the cell membrane in Brachidontes virgiliae
(present study) and M. galloprovincialis (Bernard & Hodg-
son, unpublished data), supports the suggestion of
HUMPHREYS (1967).

The follicular cells of Brachidontes virgiliae are arranged
in a manner characteristic of the bivalves (DE JONG-BRINK
etal., 1983), and these authors have reviewed the functional
roles suggested for follicle cells in the Mollusca. The cy-
toplasm of the follicle cells of B. virgiliae has large amounts
of glycogen, rough endoplasmic reticulum, and mitochon-
dria. The rough endoplasmic reticulum lies close to the
cell membrane of the developing oocyte, suggesting that
the follicle cells may play a significant role in the matu-
ration of the oocyte. However, the exact function of the
follicle cells of B. virgiliae remains to be elucidated.

The working temperatures and salinity used in the in
vitro embryonic development studies were selected on the
basis of data generated by HOWARD-WILLIAMS (1976, 1978)
for Swartvlei. During the mouth-open phase of the lake,
surface and mid-column salinities varied between 9 and
15%, with the lowest end of the range occurring for 8 of
17 months of study, and the highest for 3. Temperatures
varied between 14 (June-October, winter-spring) and 24°C
(December-March, summer) during the same 17-month

Page 287

Table 1

Summary of the in vitro early development of Brachidontes
virgiliae at 24°C and a salinity of 9%o.

Time* Development stage Figure
5 min Polar body extrusion 13A
25 min First cleavage, micro- and megamere pro- 13A
duction
70 min 3-cell stage developing 13A
80 min 4-cell stage 13A
115 min 8-cell stage; pronounced dexiotropic
cleavage
130 min 32-cell stage
4h Early blastula free of the vitelline mem- 13B
brane
5h Blastopore closing after epibolic gastrula- 13C
tion. Morula performing limited spiral
movements; ectodermal cilia short.
10h Development of velar cirri
13-15h Developing velum; digestive system devel- 14B
oping, directed swimming.
20h Velar resorption commences; shell and 14C
hinge forming; characteristic bilateral
symmetry.
23-24 h Free-swimming spat; shell well devel- 14D

oped, adductor muscles forming; ciliat-
ed foot; avoidance response to distur-
bance.

* Average development time from fertilization.

study period. Development of the mussel is very rapid at
24°C (fertilization to spat within 24 h) and is still relatively
rapid at 15°C, while the difference in development time
between 20 and 24°C (ca. 10 h) is, perhaps, surprising
given the temperature variation overlap during the exper-
iments.

COETZEE (1978) has recorded high densities of “‘lamel-
libranch veliger larvae” in Swartvlei (Brachidontes virgiliae
is the only possible source) between spring and early sum-
mer (October-December, with a peak of >40,000 m~? at
6 m depth) and in autumn (April-May, between 37,000
and 39,000 m~?). Spatfall on the submerged plant Pota-
mogeton pectinatus reached >2.5 million individuals m~?
of lake bed in November 1978 and >1.25 million indi-
viduals m~? in April (autumn) 1978 (Davies, unpublished
data), confirming the main reproductive periods of B. vir-
giliae within the system. The double peak of spatfall is
difficult to explain in terms of the ecology of the animal,
particularly as the autumnal peak occurs as temperatures
are falling within the system, and as the Potamogeton com-
munity is beginning to senesce (with concomitant loss of
the enormous area available for attachment of B. virgiliae).
Mortality must be very large indeed at this time.

The standing stocks of Brachidontes virgiliae within
Swartvlei are enormous (BOLTT, 1973; DAviEs, 1982,
1984). Indeed, they may constitute the highest standing

Page 288

The Veliger, Vol. 30, No. 3

Figure 14

Photomicrographs of development of veliger and spat at 24°C and 9%o. Scale bars = 10 um. A. Early veliger some
5h post-fertilization showing development of ectodermal cirri (arrow). B. Veliger at between 5 and 10 h post-
fertilization showing development of velar cirri (V) and early organ differentiation (arrow). C. Early spat with
pronounced bilateral symmetry showing development of the adductor muscles (AM) and the dorsal aspect of the
valves. D. Fully developed spat showing the hinge ligament (arrow), shell (Sh), and developing foot.

stocks of any invertebrate in any aquatic ecosystem any-
where in the world (DAVIES, 1982). Such densities may
be a function of the ability of the mytilid to live attached
to vertical surfaces (DAVIES, 1982, 1984). In the context
of the annual cycle of Potamogeton (e.g., HOWARD-
WILLIAMS, 1978), the availability of a large area of sub-
stratum for attachment is temporally limited. This may

account for the small size and early reproductive behavior
of B. virgiliae populations in Swartvlei, as compared to
populations from the estuaries of the eastern Cape. In
Swartvlei, the animal is capable of commencing gamete
production at 5-6 mm shell length (maximum shell length
in Swartvlei = 12 mm) and development to the settling
spat stage at ambient temperatures is rapid. By comparison

Reb keeBernarduchal 988

Table 2

Summary of the in vitro early development of Brachidontes
virgiliae at 15 + 2 and 20 + 2°C and a salinity of 9%o.

Development time from fertilization

Development stage 15°C 20°C
Polar body extrusion 25 min 8 min
First cleavage 90 min 40 min
3-cell stage 3 h 30 min 100 min
4-cell stage 5h 160 min
8-cell stage 12h 3h 15 min
32-cell stage 14h 4h
Early blastula ca. 19h 9h
Gastrulation ca. 23h ca.12h
Early veliger ca. 31h 20h
Mature veliger ca. 38h 24h
Velar resportion ca. 48 h ca. 30h
Spat ca. 56h ca. 36h

Figure 15

Diagrammatic representation of the structure of the spermato-
zoon of A, Musculus discors (after FRANZEN, 1983), and B, Brach-
idontes (Musculus) virgiliae (present study). Scale bar = 1 um.

Page 289

populations found at the head of the Kowie estuary, where
the substratum for attachment is limited to the protected
undersurfaces of relatively large boulders, B. virgiliae grows
to 30 mm shell length, but does not produce gametes until
the shell is approximately 10 mm long. Densities and
standing stocks are also very low (DAVIES, 1980, unpub-
lished data). In addition to further studies on the taxonomic
position of the species, possibly using the structure of the
spermatozoon as a basis, information is also required on
its growth, fecundity, and food requirements, together with
a comparison between estuarine and coastal lake popu-
lations, in order to gain insight into the biology of this
remarkable animal.

ACKNOWLEDGMENTS

The work on gametogenesis and gamete structure was
supported by a grant from Rhodes University. Studies on
the embryonic development of Brachidontes virgiliae were
supported by the South African Council for Scientific and
Industrial Research, Pretoria. These funding agencies are
gratefully acknowledged. We would like to thank Mr. R.
H. M. Cross for photographic assistance.

LITERATURE CITED

Apiyopl, K. G. & R. G. Abiyop! (eds.). 1983. Reproductive
biology of invertebrates. Vol. II. Spermatogenesis and sperm
function. John Wiley & Sons Ltd.: Chichester. 692 pp.

ALLANSON, B. R. 1981. The coastal lakes of southern Africa.
Pp. 331-344. In: J. H. Day (ed.), Estuarine ecology, with
particular reference to southern Africa. A. A. Balkema: Cape
Town.

ANDERSON, E. 1969. Oocyte-follicle cell differentiation in two
species of amphineurans (Mollusca), Mopalia mucosa and
Chaetopleura apiculata. Jour. Morphol. 129:89-126.

BacceTTl, B. 1979. The evolution of the acrosomal complex.
Pp. 305-329. In: D. W. Fawcett & J. M. Bedford (eds.),
The spermatozoon. Urban and Swartzenberg: Baltimore.

BARNARD, K.H. 1964. Contributions to the knowledge of South
African marine Mollusca. Part V. Lamellibranchiata. Ann.
So. Afr. Mus. 47(3):361-593.

BEAMS, H. W. & S. S. SEKHON. 1966. Electron microscope
studies on the oocyte of the fresh water mussel (Anodonta),
with special reference to the stalk and mechanism of yolk
deposition. Jour. Morphol. 119:477-502.

BERNARD, R. T. F.& A. N. HopGson. 1985. The fine structure
of the sperm and spermatid differentiation in the brown
mussel Perna perna. So. Afr. Jour. Zool. 20:5-9.

BotTT, R. E. 1973. Coastal lakes benthos. 3 pp. Jn: Report of
the Institute for Freshwater Studies, Annual Reports and
Reprints, 1972/3, Rhodes University, Grahamstown.

CoETZEE, D. J. 1978. The zooplankton of the Wilderness
Lakes. Ph.D. Thesis, University of Stellenbosch. 167 pp.

Davies, B. R. 1980. The identification of the mytilids Musculus
virgiliae Barnard, Arcuatula capensis (Krauss) and Brachi-
dontes variabilis Krauss, with corrections to the literature and
a note on their distribution. Trans. Roy. Soc. So. Afr. 44:
225-236.

Davies, B.R. 1982. Studies on the zoobenthos of some southern
Cape coastal lakes. Spatial and temporal changes in the
benthos of Swartvlei, South Africa, in relation to changes in
the submerged littoral macrophyte community. Jour. Lim-
nol. Soc. So. Afr. 8:33-45.

Page 290

Davies, B. R. 1984. The zoobenthos of the Touw River Flood-
plain. Part 1: The benthos of the Wilderness Lagoon, Touw
River and the Serpentine, and the effects of submerged plant
cutting. Jour. Limnol. Soc. S. Afr. 10:62-73.

DE JONG-BRINK, M., H. H. BOER & J. JoossE. 1983. Mol-
lusca. Pp. 297-355. In: K. G. Adiyodi & R. G. Adiyodi
(eds.), Reproductive biology of invertebrates. Vol. 1. John
Wiley & Sons Ltd.: Chichester.

Franzen, A. 1983. Ultrastructural studies of spermatozoa in
three bivalve species with notes on evolution of elongated
sperm nucleus in primitive spermatozoa. Gamete Res. 7:
199-214.

Hopecson, A. N. & R. T. F. BERNARD. 1986. Observations on
the ultrastructure of the spermatozoon of two mytilids from
the south-west coast of England. Jour. Mar. Biol. Assoc.
U.K. 66:385-390.

HOWARD-WILLIAMS, C. 1976. Swartvlei project. Background
data on physical, chemical and biological aspects of the pe-
lagic and littoral zones of Swartvlei November 1974—-March
1976, and recommendations for future research. Institute for
Freshwater Studies, Rhodes University, Grahamstown. 29
PP-

HOwWARD-WILLIAMS, C. 1978. Growth and reproduction of
aquatic macrophytes in a south temperate saline lake. Ver-
handlungen, Internationale Vereinigung ftir theoretische und
angewandte Limnologie 20:1153-1158.

Humpureeys, W. J. 1962. Electron microscope studies on eggs
of Mytilus edulis. Jour. Ultrastr. Res. 7:467-487.

Humpureeys, W. J. 1967. The fine structure of cortical granules
in the eggs and gastrulae of Mytilus edulis. Jour. Ultrastr.
Res. 17:314-326.

KILBURN, R. & E. Rippey. 1982. Sea shells of southern Africa.
Macmillan: Johannesburg. 249 pp.

The Veliger, Vol. 30, No. 3

LonGo, F. J. & E. J. DORNFELD. 1967. The fine structure of
spermatid differentiation in the mussel Mytilus edulis. Jour.
Ultrastr. Res. 20:462-480.

McLaren, E. C.K. 1977. Predation by the crab Scylla serrata
(Forskal) on the sessile bivalves Musculus virgiliae Barnard
and Lamya capensis (Krauss). Unpubl. B.Sc. Honours Proj-
ect, Rhodes University, Grahamstown.

NORREVANG, A. 1968. Electron microscopic morphology of oo-
genesis. Inter. Rev. Cytol. 23:113-186.

PLUMSTEAD, E. 1976. ’n Inleidende studie van die groei, re-
produksie en osmoregulering van Musculus vigiliae (sic!). Un-
publ. B.Sc. Honours Project, University of Port Elizabeth.

PopHaM, J. D. 1979. Comparative spermatozoon morphology
and bivalve phylogeny. Malacolog. Rev. 12:1-20.

SHARP, B. J. 1977. The feeding and distribution of Musculus
virguiae Barnard in the Kowie Estuary, South Africa. Un-
publ. B.Sc. Honours Project, Rhodes University, Grahams-
town.

TayLor, G. T. & E. ANDERSON. 1969. Cytochemical and fine
structural analysis of oogenesis in the gastropod Ilyanassa
obsoleta. Jour. Morphol. 129:211-248.

THORSON, G. 1935. Biologische Studien uber die Lamelli-
branchier Modiolaria discors L. und Modholaria nigra Gray
in Ostgronland. Zoologischer Anzeiger 111:297-304.

WHITFIELD, A. K. 1982. Trophic relationships and resource
utilization within the fish communities of the Mhlanga and
Swartvlei estuarine systems. Ph.D. Thesis, University of
Natal, Pietermaritzburg. 157 pp.

WHITFIELD, A. K. 1984. The effects of prolonged aquatic
macrophyte senescence on the biology of the dominant fish
species in a southern African coastal lake. Estuar. Coast.
Shelf Sci. 18:315-329.

The Veliger 30(3):291-294 (January 4, 1988)

THE VELIGER
© CMS, Inc., 1988

Effect of Eyestalk Ablation on Oviposition in the

Snail Lymnaea acuminata

S. K. SINGH anp R. A. AGARWAL

Department of Zoology, University of Gorakhpur, Gorakhpur 273009 U.P., India

Abstract.

The effects of eyestalk ablation on spawning in normal as well as cyclophosphamide-

injected Lymnaea acuminata are reported. Unilateral or bilateral ablation of the eyestalk induced a spurt
of spawning in snails. A second spurt of spawning could be induced in unilaterally ablated snails when
the eyestalk of the other side was removed. Administration of cyclophosphamide, on the other hand,
considerably reduced spawning. Eyestalk ablation, however, even in cyclophosphamide treated snails,
stimulated egg laying to a considerable extent. It is proposed that, whereas the effect of cyclophosphamide
is directly on the gonads, eyestalk ablation induces spawning through an endocrine mechanism.

INTRODUCTION

Information on the physiology of reproduction in pul-
monate snails is fairly extensive; among these, the fresh-
water snail Lymnaea stagnalis (Basommatophora) has been
studied in detail. The endocrine control of reproduction in
the Basommatophora has been reviewed by JOOSSE &
GERAERTS (1983) and GERAERTS & JOOSSE (1984). Ac-
cording to these authors, separate mechanisms regulate
male and female systems in the hermaphrodite snail L.
stagnalis. Specific neurohormones for the control of ovu-
lation and the preparation of the egg mass have been sug-
gested in these snails. In the stylommatophorans, optic
tentacles are a source of an androgenic factor (RUNHAM,
1983) which helps in the differentiation of male sex cells.
SINGH & AGARWAL (1981, 1983) demonstrated that in-
jection of cyclophosphamide caused sterility in another
hermaphrodite snail, L. acuminata.

In the present study the effect of eyestalk ablation on
ovulation was studied in Lymnaea acuminata. Investiga-
tions were carried out on normal as well as on snails made
sterile by the injection of cyclophosphamide (SINGH &
AGARWAL, 1981, 1983). These studies have practical sig-
nificance in that this snail is the intermediate host of the
parasites Fasciola gigantica and F. hepatica which cause
endemic fascioliasis in sheep and cattle.

MATERIALS anp METHODS

Adults of Lymnaea acuminata (2.6 + 0.3 cm length) were
collected from local freshwater ponds and kept in glass
aquaria for 24 h in order to acclimatize them to laboratory

conditions. Thereafter, the effect of eyestalk ablation on
egg laying was studied in normal and cyclophosphamide
injected snails. Groups of 20 snails were kept in 10-L
capacity glass aquaria containing 3 L of dechlorinated tap
water.

Egg masses of Lymnaea acuminata, which are laid in
the form of gelatinous ribbons consisting of 5-120 eggs
each, were collected every 24 h from the aquaria and
transferred to 10-cm diameter petri dishes for counting the
number of eggs. For ablation, the animals were gently
picked out of an aquarium and either one or both eyestalks
were quickly snipped off with a pair of iris scissors. An-
imals were then returned to the aquarium. Controls were
likewise sham-operated on the foot.

Solutions of the desired strength of cyclophosphamide
were prepared in distilled water and 50 wL was injected
in the foot of the snails with an “Agala” micrometer syringe
(SINGH & AGARWAL, 1981). Controls received distilled
water alone.

Every experiment was conducted for six days on five
groups of 20 snails each. Group A consisted of untreated
controls; group B contained sham-operated controls kept
in total darkness; group C consisted of eyestalk-ablated
snails; group D consisted of ablated snails that were given
7 ug cyclophosphamide/snail daily for the first three days;
group E received 7 ug of cyclophosphamide/snail daily for
the first three days, following which their eyestalks were
ablated.

Two sets of experiments were also conducted to study
the effect of unilateral ablation. In one set, the left eyestalk
was ablated and in the other set the right eyestalk was

Page 292 The Veliger, Vol. 30, No. 3

Table 1

Effect of sham-operation, absence of light, and eyestalk ablation on egg laying in the snail Lymnaea acuminata. Table

shows number of spawns and number of eggs laid by groups of 20 snails. Each value represents mean + SE of 6 replicates

with 20 snails in each replicate. Student’s ¢-test were applied between the control and ablated snails to locate significant
differences.

Sham-operated (kept in

Control (group A) darkness) (group B) Bilaterally ablated (group C)

Number of Number of Number of
Period spawns Number of eggs spawns Number of eggs spawns Number of eggs
24h 7.23 22023 iISO0sC6 ss 5.37 5.66 + 0.36* IS s2 757 18.83 + 0.91* 532.5 + 29.12*
48h 5.83 + 0.18 148.66 + 3.32 6.00 + 0.40 129.66 + 8.47 6.5 + 0.54 154.5 + 8.34
72h 7.00 + 0.28 131.32 + 1.25 5.5 + 0.37* 126.00 + 5.78 3.83 + 0.33* 92.83 + 5.39*
96h ©.35) as O23 126.5 + 4.77 5,5) 22 0.37/ IDs) 22 7/13) 2s) as Of" 4.33) as 8/7"
120 h 6.33 + 0.23 143.83 + 9.31 5.33 + 0.36 135.5 + 8.68 1.66 + 0.36* 17.66 + 4.06*
144h 6.16 + 0.18 140.00 + 3.29 5.33 + 0.46 132.16 + 3.36 0 0
Total number of eggs
in 144h 838 790 836

* Significantly (P < 0.05) different from control of corresponding period.

ablated. Controls were sham-operated as before. The eggs
laid in both sets of unilateral ablation experiments were
observed for 72 h. After this the eyestalk of the other side
was also ablated and egg laying was studied for the next
i2uhe

600

RES

500

400

Number Of Eggs

Time (hours)
Figure 1

Graph showing effect of eyestalk ablation on pattern of egg laying
in Lymnaea acuminata during 144-h period. Eggs were counted
every 24 h. Data are mean of 6 replicates with 20 snails in each
replicate. Zero time indicates number of eggs laid during the 24
h preceding ablation. Eyestalk of one side was removed and eggs
were counted for the next 72 h; this was followed by removal of
the eyestalk of the other side, with eggs counted for the subsequent
72 h. LES: initially left eyestalk was ablated, 72 h after which
right eyestalk was ablated. RES: initially right eyestalk was
ablated, 72 h after which left eyestalk was ablated.

Every experiment was replicated six times. Student’s
t-tests were applied to detect significant (P < 0.05) changes.

RESULTS

Groups of 20 normal Lymnaea acuminata together laid
approximately 140 eggs/day during the six day observa-
tion period. An average of approximately 6 snails out of
the group of 20 spawned every day (Table 1), indicating
that over the entire observation period of 144 h each snail
spawned approximately twice. The number of eggs laid
by sham-operated controls kept in darkness did not differ
significantly from non-operated controls kept in lighted
aquaria (Table 1).

Bilateral removal of the eyestalks resulted in a sudden
spurt of egg laying; during the first 24 h after eyestalk
ablation an average of 18.83 spawns were laid. The num-
ber of eggs on the first day of ablation was 532 as compared
to 150 in non-ablated snails (Table 1). This brisk rate of
spawning, however, tapered off to no egg laying by the
sixth day. The difference in the number of eggs between
control and ablated snails was significant on five of six
days (P < 0.05; t-test). The total number of eggs, however,
laid by 20 snails in 144 h was 836 in the case of ablated
and 838 in the case of non-ablated snails.

With unilateral eyestalk ablation also, there was a spurt
of egg laying immediately after one of the eyestalks was
removed. This started tapering off by the third day (Figure
1). Removal of the eyestalk on the other side, after 72 h,
started a second spurt of egg laying (Figure 1). Thus, when
the right eyestalk was removed 481 eggs were laid on the
first day, 151 on the second, and 78 on the third. Removal
of the other eyestalk resulted, after 24 h, in the laying of
273 eggs on the fourth day (Figure 1). Figure 1 also shows
that right or left eyestalk ablation had the same effect on

egg laying.

S. K. Singh & R. A. Agarwal, 1988 Page 293

Table 2

Effect of cyclophosphamide treatment (7 wg/animal/day) and eyestalk ablation on egg laying in Lymnaea acuminata.

Values are mean + SE of 6 replicates of 20 snails each. All snails were injected with cyclophosphamide at 7 ug/day/

animal for the first 3 days. Group D was ablated at the start of the experiment. Group E was ablated after 72 h. Student’s
t-test were applied to locate significant differences.

Ablated after 72 h (cyclophosphamide injected for
the first 3 days) (group E)

Ablated on 1st day (cyclophosphamide injected
for the first 3 days) (group D)

Period Number of spawns Number of eggs Number of spawns Number of eggs
24h 8.16 + 0.35 177.16 + 8.98F 4.16 + 0.18*,F 72.33 + 1.80*,
48 h 4.5 + 0.24f 88.5 + 2.93 B83) se Oa a Aiejasle) as Oey
72h 3.16 + 0.33 BAIS 25 O62h; 2.16 + 0.33* 22.16 + 4.54* Ff

(ABLATION)
96h 0 0 8.16 + 0.44* F 170.16 + 5.13*,F
120 h 0 0 4.00 + 0.28*,F 86.33 + 3.07*,F
144h 0 0 0 0

* Group E significantly (P < 0.05) different from group D.
} Significantly different from controls (Table 1).

Injection of cyclophosphamide at a dose of 7 wg/day for
three days significantly (P < 0.05) reduced the number of
eggs (Table 2). Thus, when cyclophosphamide was in-
jected into non-ablated snails, the total number of eggs
produced by 20 snails during the first three days was 137
as compared to 429 in control snails (Tables 1, 2). Injection
of cyclophosphamide into ablated snails also reduced the
number of eggs, but the reduction was significantly less
than that observed in non-ablated snails during the first
three days. In cyclophosphamide injected snails, however,
oviposition ceased after three days (Table 2).

Eyestalk ablation, even in snails treated with cyclo-
phosphamide for the first three days, resulted in a second
spurt of egg laying for two days (Table 2). However, these
eggs did not develop into young.

DISCUSSION

The present study clearly shows that ablation of the eye-
stalk(s) of Lymnaea acuminata initiates vigorous spawning
activity within 24 h. In the beginning, the rate of ovipo-
sition was nearly 3.5 times higher than controls. From the
number of spawns, eyestalk ablation apparently caused
immediate spawning in nearly all of the snails. The rate
of egg laying, however, gradually declined so that in the
operated snails oviposition stopped completely after 120
h, even though the control snails continued to lay approx-
imately the same number of eggs throughout the obser-
vation period. The present study also demonstrates that,
even though eyestalk ablation changed the pattern of egg
laying, the total number of eggs laid during the six day
observation period was the same in both groups. Indeed,
eyestalk ablation, although it causes a sharp increase in
the rate of delivery of eggs immediately after ablation, did
not cause any net increase in the number of eggs laid.
Data presented in this study shows that there was no

change in the egg-laying pattern of sham-operated snails
kept in total darkness. This rules out the possibility of
blindness or injury being the cause of the egg-laying stim-
ulus. Indeed, our study on unilateral ablation shows that
removal of only one eyestalk of either side can cause in-
creased egg laying. Moreover, a second spurt of spawning
could be successfully started by the removal of the other
eyestalk.

SINGH & AGARWAL (1981, 1983) demonstrated that the
alkylating drug cyclophosphamide is a potent chemoster-
ilant for Lymnaea acuminata. The present data show that
ablation of eyestalks even in cyclophosphamide-treated
snails caused a two-day spurt of egg laying. Since ablation
can induce egg laying even in cyclophosphamide treated
snails it is possible that ablation and cyclophosphamide
act at different sites. SINGH & AGARWAL (1981, 1983)
reported that cyclophosphamide reduced the DNA and
RNA levels in the ovotestis of L. acuminata, thus indicating
that the drug acts directly on gonads. It seems that ablation,
which increases spawning in normal as well as in cyclo-
phosphamide-injected snails, does not affect the gonads
directly but through the neurohumoral system. Increased
oviposition following ablation, three days after cyclophos-
phamide injection, also suggests that eyestalk removal can
trigger the neurohumoral system even in sterile snails.
There are a number of reports (MAAT et al., 1983;
SCHEERBOOM, 1978; JOOSSE & VELD, 1972; BOHLKEN &
JoossE, 1982) that the caudo-dorsal cells in L. stagnalis
release an ovulation hormone. It is possible that removal
of the eyestalks in L. acuminata also stimulates the caudo-
dorsal cells to release this hormone.

LITERATURE CITED

BOHLKEN, S. & J. JoossE. 1982. The effect of photoperiod on
female reproductive activity and growth of the freshwater

Page 294

pulmonate snail Lymnaea stagnalis kept under laboratory
breeding conditions. Int. Jour. Invertebr. Reprod. 4:213-
222.

GERAERTS, W. P. M. & J. JoossE. 1984. Freshwater snail
(Basommatophora). Jn: K. M. Wilbur, A. S. Tompa, N. H.
Verdonk & J. A. M. Van Den Biggelaar (eds.), The Mol-
lusca 7:142-199. Academic Press, Inc.: New York.

JoossE, J. & W. P. M. GERAERTS. 1983. Endocrinology. Jn:
A. S. M. Saleuddin & K. M. Wilbur (eds.), The Mollusca
4:318-390. Academic Press, Inc.: New York.

JoossE, J. & C. J. VELD. 1972. Endocrinology of reproduction
in the hermaphrodite gastropod Lymnaea stagnalis. Gen.
Comp. Endocrinol. 18:599-600.

Maat, A. T., J. C. LODDER & M. WILBRINK. 1983. Induction
of egg-laying in the pond snail Lymnaea stagnalis by envi-
ronmental stimulation of the release of ovulation hormone

The Veliger, Vol. 30, No. 3

from caudo-dorsal cells. Int. Jour. Invertebr. Reprod. 6:239-
247.

RUNHAM, N. W. 1983. Mollusca, accessory sex glands. In: K.
G. Adiyodi & R. G. Adiyodi (eds.), Reproductive biology of
invertebrates. Wiley: England.

SCHEERBOOM, J. E. M. 1978. The influence of food quantity
and food quality on assimilation, body growth and egg pro-
duction in the pond snail Lymnaea stagnalis (L.), with par-
ticular reference to the haemolymph-glucose concentration.
Proc. K. Acad. Wet. C81:173-183.

SINGH, R. & R. A. AGARWAL. 1981. Cyclophosphamide as a
potential chemosterilant for harmful snails. Acta Pharmacol.
Toxicol. 49:195-199.

SINGH, R. & R. A. AGARWAL. 1983. Chemosterilization and
its reversal in the snail Lymnaea acuminata. Acta Pharmacol.
Toxicol. 52:112-120.

The Veliger 30(3):295-304 (January 4, 1988)

THE VELIGER
© CMS, Inc., 1988

A Review of the Genus Agaronia (Olividae) in the

Panamic Province and the Description of

Two New Species from Nicaragua

by

AL LOPEZ,'! MICHEL MONTOYA,?? anp JULIO LOPEZ!

' Universidad Centroamerica (UCA), P.O. Box A-90, Managua, Nicaragua
* Interamerican Institute for Cooperation on Agriculture (IICA),
P.O. Box 4830, Managua, Nicaragua

Abstract.

Three previously recognized Panamic species, Agaronia testacea (Lamarck, 1811), A. pro-

patula (Conrad, 1849), and A. griseoalba (von Martens, 1897) (senior synonym here replacing A. murrha
Berry, 1953), are reviewed and their occurrences reported for the Panamic province. Two new species,
A. mca and A. jesuitarum, are described, primarily from records in Nicaragua. Species are defined
using parameters of protoconch type, spire height, aperture width, pillar lirae count, and shell length.
Two distinct kinds of protoconch—acuminate and mammillate—are distinguished: species with acu-
minate protoconchs are A. testacea, A. propatula, and A. jesuitarum; those with mammillate protoconchs

are A. griseoalba and A. nica.

INTRODUCTION

Two species, Agaronia testacea (Lamarck, 1811), and A.
propatula (Conrad, 1849), have been regarded as broadly
distributed in the Panamic province (see KEEN, 1958, 1971).
A third species, A. murrha Berry, 1953, has been cited by
Keen as known only from Corinto, Nicaragua. Previous
authors have not realized that the latter species is broadly
distributed in the southern Panamic province and has an
older name. The extent to which the same patterns of color
variation are shared by co-occurring species has not been
understood. Here we demonstrate, based on meristic char-
acters, that there are five Panamic species, two of which
are new.

MATERIALS anp METHODS

The identity of previously described taxa presented a prob-
lem only for one of the names introduced by VON MARTENS,
1897: Oliva (Agaronia) testacea var. griseoalba. The type
specimen was received on loan from the Zoologisches Mu-
seum of Humboldt-Universitat in Berlin (ZMB) by Dr.
McLean at the Los Angeles County Museum of Natural
History, where it was photographed for inclusion here.

* Present address: P.O. Box 6327, San José, Costa Rica.

Von Martens also proposed Oliva (Agaronia) testacea mut.
candida, but that name is preoccupied by Oliva candida
Lamarck, 1811, and need not be considered.

Specimens were collected by us at low tide and by wad-
ing and snorkling at a number of localities in Nicaragua
and Costa Rica (Table 1). Information provided by Dr.
McLean about the occurrences of these species elsewhere
in the Panamic province is also included. We have also
examined specimens received on loan from Carol Skoglund
of Phoenix, Arizona, and David G. Robinson of Tulane
University, New Orleans, Louisiana. Voucher specimens
of previously described species and type specimens of the
new species have been placed in the following institutional
collections: CAS—California Academy of Sciences, San
Francisco, California; LACM—Los Angeles County Mu-
seum of Natural History, Los Angeles, California; LSM—
La Salle Museum of Natural History, San José, Costa
Rica; UCA—Central America University, Managua, Nic-
aragua; UCRZ— Zoology Museum of University of Costa
Rica, San Jose.

The meristics are based on 38 specimens of each of the
five species. Measurements were made with vernier cali-
pers, with an accuracy of 0.05 mm. Abbreviations for the
physical parameters (Figures 1, 2, and text) are as follows:
a, lateral spire height from tip of callus above aperture to
protoconch tip; 6, width, maximum distance from labrum

Page 296

to opposite side; c, crest on fasciolar band; d,, distance
along labrum from suture to fasciolar band; d,, same dis-
tance (suture to fasciolar band) on side opposite from lip;
e, edge of pillar pleats; f, spire factor, a/w, a measure of
spire acuteness; g, breadth factor, o//, a measure of ap-
erture width; h, maximum height; &, dorsal color band; J/,
length of shell from protoconch to tip of columella; n,
number of specimens examined; 0, maximum aperture
width from tip of penult pillar pleat to edge of labrum; #,
pillar pleats; 7, relative growth factor d,/d,, a measure of
relative growth of shell length; SD, standard deviation; s,,
posterior pillar lirae; 5s, anterior pillar lirae; ¢, terminal
pleat; w, width of diameter of spire base measured from
tip of callus above aperture to opposite point on suture.

SYSTEMATIC TREATMENT
Family OLIVIDAE Latreille, 1825
Subfamily AGARONIINAE Olsson, 1956

Genus Agaronia Gray, 1839

Type species (monotypy): Voluta hiatula Gmelin, 1791. Re-
cent, west Africa.

The shell is medium thick, ovate-fusiform, with a trun-
cate flaring aperture extending about 0.7 of shell length.
One strong terminal pleat (¢) extends internally from the
pillar through the spire whorls. Separated from it by a
sulcus are 8 to 20 lirae on the inner surface of the pillar
and the anterior parietal callus. The count of lirae provides
a useful specific character. Some of these lirae are engraved
and prolonged into the fasciole as strong pleats (p) over
the pillar. The highest of these usually marks the posterior
limit of the anterior pillar lirae (s,), but more posteriorly
there are a few posterior pillar lirae (s,), particularly on
Agaronia griseoalba. The average number of lirae, including
the terminal pleat, varies from a minimum of 9.1 for A.
propatula to a maximum of 16.7 for A. griseoalba. The
slightly raised callus pad on the pillar and fasciole is mi-
croscopically wrinkled, white, sometimes suffused with
purple. There is wide fasciolar band, covered with callus,
that forms the base of the shell. The morphology of the
fasciolar band is similar to that seen in the genus Ancilla
Lamarck, 1799, which has an “‘ancillid” band and a fas-
ciolar band separated by the “posterior fasciolar groove”
(KILBURN, 1981). In Agaronia the two bands are fused
together, but a very slight crest (c) corresponding to the
posterior fasciolar groove of Ancilla is present. The callus
of the fasciolar band is the same color as the spiral band
callus, and both often have a slightly uneven surface, var-
iegated with streaks of a different color. A short distance
above the fasciolar band there is a dorsal color band (k),
white or light purple, most easily seen on dark shells. Its
background color is made up of a closely knit web of
microscopic zigzag lines overset with larger, thin irregular
streaks that are visible without magnification. These streaks
are contained within the limits of the dorsal color band,
but in large shells they sometimes occur on other parts of

The Veliger, Vol. 30, No. 3

Table 1

Latitude and longitude of collecting localities.

N latitude W longitude
Nicaragua
Cosiguina, Chinandega 13°03'00” 87°34'00"
Jiquilillo, Chinandega 12°45'00” 87°31'30”
Aposentillo, Chinandega LAS SD” 87°21'55"
Aserradores, Chinandega 12°36'27” 87°20'37"
Corinto, Chinandega 12°30'00” 87°10'00"
Poneloya, Leon LVEDD SS” 87°02'49”
Los Playones, Leon 12°07'02” 86°44'42”
Masachapa, Managua 11°47'13” 86°31'01”
Pochomil, Managua 11°47'00” 86°30'30”
La Boquita, Carazo 11°40'40” 86°22'30”
Huehuete, Carazo 11°36'59” 86°19'34”
Chococente, Carazo 11°32'06” 86°11'15”
Rio Escalante, Rivas 11°31'04” 86°10'13”
Boca de Brito, Rivas 11°20'33” 85°58'37”
Majagual, Rivas Meee” 85°55'00”
Marsella, Rivas 11°17'06” 85°54'14”
El Toro, Rivas 11°16’30” 85°53'59"
San Juan del Sur, Rivas 11°15'34” 85°52/49”
La Flor, Rivas 11°08'05” 85°47'38”
Ostional, Rivas 11°06'30” 85°46'00”
Costa Rica
Playas del Coco, Guanacaste 10°33'32” 85°42'08”"
Tamarindo, Guanacaste 10°18'07” 85°50'29”
Puntarenas, Puntarenas 9°58'52” 84°49'11”
Tivives, Puntarenas 9°52'10” 84°42'04"
Tarcoles, Puntarenas 9°45'49” 84°37'53”
Montezuma, Puntarenas 9°39'28" 85°04'17”
Jaco, Puntarenas 9°36'31” 84°37'30"
Esterillos, Puntarenas 9°31'31” 84°30'26"
Manuel Antonio, Puntarenas 9°23'42" 84°09'13”
Dominical, Puntarenas Py aa 83°50'57”

the dorsum. The surface of Agaronza is smooth and shiny,
but not highly glazed except where covered with callus.
The interior is dark purple in some shells and light purple,
yellow, or white in other specimens, often with two well-
marked purple bands. The edge of the lip reveals the color
of the dorsum along its length.

The height and shape of the spire is important as a
specific character. The spire has a channeled suture and
three moderately callused whorls. There is a strongly
marked spiral callus and blotch of darker color that often
dips into the aperture. It is deep purple or brown on dark
shells, light purple or yellow on light shells. Sometimes a
light purple parietal blotch is apparent on fresh shells, but
this may fade with time.

The protoconch is translucent or opaque, of 2 to 2.5
whorls, generally darker than the ground color of the spire.
The protoconch is entirely devoid of sculpture, with the
almost imperceptible suture developing into a channel on
the last nepionic whorl. The contrast between the proto-
conch and the first whorl of the teleoconch is what deter-
mines a mammillate (Figure 3) or an acuminate (Figure
4) form of the protoconch. In the acuminate form, the

A. Lopez et al., 1988

Page 297

spire callus

channeled spire blotch

suture

parietal

blotch
parietal
callus

of
fasciolar SF
band

Explanation of Figures 1 and 2

Figure 1. Shell features of Agaronia: c, crest on fasciolar band;
e, edge of pillar pleats; &, dorsal band; p, pillar folds; s,, posterior
pillar lirae, s,, anterior pillar lirae; ¢, terminal fold.

increase in diameter of the whorls is gradual, so that pro-
toconch and teleoconch fuse into a smooth, continuous cone
with an angle of about 32 degrees. In the mammillate
form, the first whorl of the teleoconch is about twice the
diameter of the protoconch, which stands out nipple-like,
and the cone forms an angle of about 50 degrees in Agaronia
griseoalba and about 62 degrees in A. nica. An additional

Figure 2. Agaronia: measurements taken for statistical analysis.
See list in text.

difference between the two forms is that the diameter of
the embryonic whorl varies from 0.45 to 0.7 mm in the
three acuminate forms, A. jeswitarum, A. testacea, and A.
propatula respectively, and from 0.6 to 1.2 mm in A. nica
and A. griseoalba, the two mammillate forms.

In order to quantify the height of the spire, we define
a spire factor (f = a/w), where (a) is the lateral length of

Explanation of Figures 3 and 4

Figure 3. Protoconch, mammillate form of Agaronza nica sp. nov.
Scale bar = 1 mm.

Figure 4. Protoconch, acuminate form of Agaronia jesuitarum
sp. noy. Scale bar = 1 mm.

Page 298

The Veliger, Vol. 30, No. 3

Figure 5

SEM view of radula of Agaronia griseoalba, showing tricuspid rachidian with closely adjacent secondary cusps, and

single pair of hook-shaped lateral teeth. Scale bar = 20 um.

the spire and (w) is the diameter of the spire base, both
measured from the tip of the callus just above the aperture.
The very sharp outline of the channeled suture makes it
possible to duplicate the measurements. Average values for
the spire factor for the Panamic species vary from 1.35
(SD, +£0.07) for Agaronia testacea to 1.01 (SD, £0.04) for
A. nica. The latter has a convex spire, in contrast to the
others, which have spires with straight or concave profiles.

The foot and body of Agaronia species are white to buff,
more or less intensely speckled with purple; some animals
appear to be entirely of this color except for a white, narrow
edge around the foot. The siphon is ribbonlike but tubular,
also buff and speckled with purple, but with an orange
tip. The posterior lobe of the foot is easily broken off at a
“tear” line. The gut is dark gray with a granular white
or yellow digestive gland ventrally.

The animals live in the sand in the tidal zone. When
active, the shells are nearly completely covered by the
propodium and the parapodia. We have often seen them
feeding on Oliwella semistriata (Gray, 1839), which is abun-
dant in Nicaragua and Costa Rica, and rarely on small
Donacidae and Tellinidae. The prey is enveloped by the
foot and then the Agaronia burrows into the sand while
feeding (LOPEZ, 1978). Dissection has also revealed re-
mains of other small invertebrates in the stomach.

Contrary to previous descriptions (KEEN, 1971:625;
ABBOTT, 1974:238), Panamic Agaronia do not have an
operculum. However, A. travassos: Morretes, 1938, which
is endemic to Brazil, does have an operculum (RIos, 1975).

Radulae for all species except Agaronia testacea were
examined; that of A. griseoalba is illustrated (Figure 5).
As in all Olividae, the radula is rachiglossan with a tri-
cuspid rachidian tooth, the central cusp being slightly
smaller than the other two. Lateral to the two large cusps
are small secondary cusps; in this detail, Agaronia and
Olivancillaria d’Orbigny, 1840, differ from the rest of the

Olividae, which do not have these denticles (BURCH &
BURCH, 1964). Radulae of different Agaronia species show
no detectable differences in the shape and spacing of cusps.
In A. propatula, the external sides of the outer cusps are
aligned, giving the ribbon a more regular appearance. In
fresh specimens of A. jeswitarum, the tips of the laterals
have a marked golden hue not seen in the other species.

Only three fossil species of the Olividae have been re-
ported to date from Central America. OLSSON (1922) de-
scribed Oliva testacea var. costaricensis from the Rio Banano
Formation, now dated as being Pliocene in age, and O.
mancinella from the Pleistocene Moin Formation, both
from the Limon Province of Costa Rica. Later, WOODRING
(1964) reassigned these two taxa to the genus Agaronia
and treated both as subspecies of A. testacea. He also de-
scribed a new subspecies, A. testacea hadra from the Plio-
cene Gatun Formation of Panama. These fossil taxa need
to be reviewed, taking into account their probable descen-
dents in the Caribbean and Panamic biogeographic prov-
inces.

Key TO LIVING PANAMIC SPECIES OF Agaronia
(data from meristics under each species)

(1) Protoconch acuminate

(a) Spire very high, f= 1.4 ............ A. testacea
(lirae 10; length 34.5 mm)

(a) Gane Iie, fH 1.2 2cccavcccecs A. jesuitarum
(lirae 15; length 21.5 mm)

(c) Spire medium, f= 1.1 ........... A. propatula

(lirae 9; length 42.0 mm)
(2) Protoconch mammillate

(a) Spire medium, f= 1.1 ........... A. griseoalba
(lirae 18; length 32.0 mm)
(id) Sjoure low, jf =] 10 .occcccccccccvcsccce A. nica

(lirae 12; length 24.5 mm)

A. Lopez et al., 1988

Page 299

Agaronia testacea (Lamarck, 1811)
(Figures 6-9)

Oliva testacea LAMARCK, 1811:324; REEVE, 1850:pl. 18, fig.
36; MARRAT, 1871:26, pl. 348, figs. 334, 335.

Oliva (Agaronia) testacea: VON MARTENS, 1897:163, pl. 16,
figs. 7, 12.

Agaronia testacea: BERRY, 1953:418, text fig. 6; HERTLEIN &
STRONG, 1955:239; KEEN, 1958:422, fig. 629; BURCH
& BURCH, 1964:111, pl. 6, fig. 2; KEEN, 1971:625, fig.
1370; ABBOTT, 1974:233, pl. 13, fig. 2548; ABBOTT &
DANCE, 1982:196 [color fig.].

Agaroma reeve:. MORCH, 1860:87 [designated fig. 36 of REEVE,
1850].

Oliva (Agaronia) testacea var. philippi VON MARTENS, 1897:
165, pl. 15, figs. 13, 14.

Description: Spire straight-sided and highest among Pan-
amic agaronias; protoconch acuminate, light colored; shell
height 31-50 mm, profile subfusiform. The body color is
usually grayish brown, with axial, brown irregular lines.
The aperture is bluish white or gray, the edge of labrum
white, often stained with brown; pillar is white. The spire
callus band reaches only halfway across from suture to
suture. The callus band and the fasciolar band callus are
light brown, variegated with whitish streaks. The proto-
conch is acuminate and light colored. Spiral blotch weak
to obsolete.

Meristics (n = 38): Spire factor 1.35 (SD, £0.07); length
34.55 mm (SD, +8.56); breadth factor 0.18 (SD, +0.02);
relative growth factor 1.37 (SD, +£0.07); lirae count 9.76
(SD, +£2.59).

Distribution: Empty shells were found in fair to good
condition at nearly all sandy beaches in Nicaragua, but
always in small numbers. Most of our specimens were
collected from the northern beaches, from the Gulf of Fon-
seca to Aserradores. No live specimens were found. How-
ever, McLean reports (personal communication) that there
are numerous live-collected records from the Gulf of Cal-
ifornia and southern Mexico, as well as Panama, in the
LACM collection.

Material examined: MExIco (Skoglund collection): Ba-
hia Cholla, Sonora, 9 specimens; Playa Novillero, Nayarit,
7 specimens. NICARAGUA (UCA): Aserradores sea beach
and estero beach: 5 lots, 24 specimens. Single shells and
fragments from Cosiguina, Aserradores, Corinto, Hue-
huete, San Juan del Sur, La Flor. Costa Rica: Tamarindo
(LSM); Montezuma (UCRZ). PANAMA: Kobbe Beach, 2
specimens (Skoglund collection). Specimens from Aser-
radores had intact protoconchs and were used for spire
measurements. This is the only species of Agaronia that
we have not collected alive in Nicaragua.

Remarks: Agaronia testacea may readily be distinguished
from the other species by its medium to large size, high
spire, and accuminate protoconch.

Specimens from the Atlantic coast of Central America
identified as this species have been reported by FLUCK
(1905:18), Houprick (1968:16), OLsson & McGIntTy

(1958:17), and WOODRING (1964:281). Those that we have
collected at Moin, Puerto Limon, Atlantic coast of Costa
Rica, do not agree with A. testacea, in having lower spires,
broader apertures, and a lower count of lirae, and remain
unidentified.

The holotype of Oliva (Agaronia) testacea var. philippi
von Martens (Figure 9) is a small shell similar to those
from Panama in the LACM collection. The locality Co-
bija, in northern Chile, quoted by VON MARTENS (1897),
is obviously erroneous, as the species has not been recorded
south of Panama.

Agaronia propatula (Conrad, 1849)
(Figures 10, 11)

Oliva propatula CONRAD, 1849:280, pl. 39, fig. 7.

Agaronia propatula: KEEN, 1958:422, fig. 629; KEEN, 1971:
625, fig. 1369 [copy Conrad fig.].

Not A. propatula of HEMMEN, 1981:128, pl. 27 [color fig.];
of ABBOTT & DANCE, 1982:196 [color fig.]. [=A. gri-
seoalba].

Description: This is the largest and most massive of the
Panamic agaronias. The spire is medium high, concave
over the aperture owing to overhang of heavy callus, pro-
toconch acuminate. Shell length about 42 mm, profile in-
flated, most globose of the five species. Lirae count lowest,
about 9. The body color is often gray with dark gray
zigzags, but it can also be light brown or terracotta marked
by gray or brown axials that score the growth lines, giving
the shell a woodlike appearance. These growth lines are
somewhat sinusoid, as is the edge of the lip, especially in
large specimens. The fasciolar band and the spire callus
are dark purple-brown and highly glazed, this callus not
reaching all the way from suture to suture on the spire
and being variegated with whitish streaks. The aperture
is bluish white or gray, the inner edge of the labrum whitish
brown. The dorsal color band is white or purple, often
with a blend of both. The protoconch is dark brown, con-
trasting with the first teleoconch whorl, which is usually
white. The spiral blotch is dark brown, strongly marked,
dipping well into the aperture, and extending along the
spire callus.

Meristics (n = 38): Spire factor 1.11 (SD, +0.08); shell
length 42.31 mm (SD, +10.66; breadth factor 0.22 (SD,
+0.01); relative growth factor 1.56 (SD, +£0.07); lirae
count 9.1 (SD, +1.66).

Distribution: Only a few live shells were taken at San
Juan del Sur, La Flor, Chococente, and Poneloya in rela-
tively coarse sand. Empty shells were found at many sandy
beaches, especially at Aserradores. KEEN (1971) gave the
range as southern Mexico to Ecuador. McLean reports
(personal communication) that the LACM collection con-
tains 9 lots of dead-collected specimens ranging from Gua-
temala to Panama.

Material examined: Mexico: Bahia de Los Angeles, Baja
California, 5 specimens (Skoglund collection); GUATE-

Page 300

The Veliger, Vol. 30, No.

Explanation of Figures 6 to 23

Figures 6-9. Agaronia testacea (Lamarck, 1811). Figure 6: LACM
127342; Aserradores, Nicaragua; length 39.6 mm. Figure 7:
LACM 127343; Bahia de Adair, Sonora, Mexico; length 50.8
mm. Figure 8: LACM 68-3; Novillero, Nayarit, Mexico; length

48.7 mm. Figure 9: Holotype, ZMB, Oliva (Agaronia) testacea
var. philippi von Martens, 1897; length 31.2 mm.

Figures 10, 11. Agaronia propatula (Conrad, 1849). Figure 10:

A. Lopez et al., 1988

MALA: San José, Escuintla, 2 specimens (D. G. Robinson
collection); NICARAGUA (UCA): Living specimens from
San Juan del Sur (2 lots); Chococente, 2 single lots; single
lots from Poneloya and La Flor. Dead shells to 65 mm in
length from Aserradores, Aposentillo, Corinto, Poneloya,
Huehuete, La Boquita, Chococente, and El Toro. No spec-
imens were found by us in Costa Rica.

Remarks: At Poneloya the living specimens occurred with
Agaronia jesuitarum. At Chococente they occurred with
A. jesuitarum, A. nica, and A. griseoalba. We found this
species to be only slightly less scarce than A. testacea.

Agaronia griseoalba (von Martens, 1897)
(Figures 12-17)

Oliva (Agaronia) testacea var. griseoalba VON MARTENS, 1897:
64, pl. 15, figs. 18, 19.

Agaronia murrha BERRY, 1953:417, pl. 29, fig. 1, text fig. 5;
HERTLEIN & STRONG, 1955:240; BURCH & BURCH, 1964:
112 [not pl. 6, fig. 4]; KEEN, 1958:422, fig. 628; KEEN,
1971:725, fig. 1368.

“A. propatula” of HEMMEN, 1981:128, pl. 27 [color fig.]; of
ABBOTT & DANCE, 1982:196 [color fig.]. Not A. pro-
patula (Conrad).

Description: Spire straight or slightly concave, medium
high, shell length about 32 mm, whorls somewhat inflated.
Protoconch mammillate, lirae count highest of the five
species, average 17, maximum 27. As noted by BERRY
(1953), the typical form is “slightly grayish porcelain-
white,” with a white, yellow, or light brown callus on
fasciole and spire, where it usually covers spire whorls
from suture to suture. The aperture is dark purple or
brown; the labrum has a white inner edge. Rarely the shell
is pink with an orange aperture, with or without two
purple bands. Variants from Costa Rica, Panama, and
Ecuador include olive-brown shells with zigzag lines and
some black shells (later turning gray) with an amorphous
white dorsal band.

Meristics (n = 38): Spire factor 1.14 (SD, +0.05); height
31.94 mm (SD, +6.99); breadth 0.19 (SD, +0.01); relative
growth factor 1.47 (SD, +0.06); lirae count 16.76 (SD,
+3.98).

—

LACM 65-88; Mata de Limon, Costa Rica; length 46.8 mm.
Figure 11: LACM 127344; Aserradores, Nicaragua; length 40.9
mm.

Figures 12-17. Agaronia griseoalba (von Martens, 1897). Figure
12: Holotype, ZMB, Oliwa (Agaronia) griseoalba von Martens,
1897, “Mexico”; length 38.4 mm. Figure 13: Holotype, CAS,
Agaronia murrha Berry, 1953; Corinto, Nicaragua; length 36.3
mm. Figure 14: LACM 127345; Huehuete, Nicaragua; length
37.2 mm. Figure 15: LACM 127346; Tivives, Costa Rica; length
39.4 mm. Figure 16: LACM 127346; Tivives, Costa Rica; length
34.7 mm. Figure 17: LACM 127346; Tivives, Costa Rica; length
35.8 mm.

Page 301

Distribution: San José, Escuintla, Guatemala, to Canoa,
Manabi, Ecuador. These represent new northern and
southern distributional records beyond those reported in
KEEN (1971).

Material examined: GUATEMALA: 1 large specimen from
San Jose, Escuintla (D. G. Robinson collection). Nica-
RAGUA (UCA): Jiquilillo, Aserradores, Corinto, Poneloya,
Huehuete, Pochomil, Chococente, Rio Escalante, Maja-
gual, Marsella, San Juan, La Flor. Costa Rica: Playas
del Coco, Puntarenas, Tivives, Tarcoles, Jaco, Esterillos,
Dominical (UCA). PANAMA: Las Lajas, Playa Jobo
(LACM). Ecuapor: Atacames, Esmeraldas (D. G. Rob-
inson collection). This is the most abundant Agaronia in
Costa Rica.

Remarks: BERRY (1953) proposed Agaronia murrha (Fig-
ure 13, holotype), from Corinto, Nicaragua, but overlooked
the prior name A. griseoalba of VON MARTENS, 1897, from
“Mexico,” which we here reinstate, based on our exam-
ination of the type specimen (Figure 12). The species has
not been frequently cited enough to warrant an effort to
conserve Berry’s name. Berry did not have material to
demonstrate the color variation possible in this species,
owing in part to the prevalence of the gray-white color
form at his type locality and most localities throughout
Nicaragua. Although he remarked in a footnote that a
dark phase seemed to be present at San Juan del Sur,
Nicaragua, these specimens prove to be A. nica, described
herein. Dark specimens of A. griseoalba (Figures 15, 16)
have the size range, the lirae count, and the mammillate
protoconch to match that of typical A. griseoalba, so there
is no possible doubt as to their identity.

Agaronia nica A. Lopez, Montoya
& J. Lopez, sp. nov.

(Figures 18-20)

“Agaronia murrha,” in part, of BERRY, 1953:419 [footnote
only]; in part of BURCH & BurRcH, 1964 [fig. 4 only].

Description: Shell solid, small, length about 25 mm, spire
low, convex, body whorl inflated, lirae count medium,
about 12. The light brown, mammillate protoconch of two

Figures 18-20. Agaronia nica Lopez, Montoya & Lopez, sp. nov.
Figure 18: Holotype, LACM 2269; San Juan del Sur, Nicaragua;
length 24.7 mm. Figure 19: LACM 127347; San Juan del Sur,
Nicaragua, collected by H. N. Lowe; length 25.5 mm. Figure
20: LACM 127348; Marsella, Nicaragua; length 23.5 mm.

Figures 21-23. Agaronia jesuitarum Lopez, Montoya & Lopez,
sp. nov. Figure 21: Holotype, LACM 2271; Poneloya, Nicara-
gua; length 21.2 mm. Figure 22: Paratype, LACM 2272; Po-
neloya, Nicaragua; length 22.6 mm. Figure 23: Paratype, LACM
2272; Poneloya, Nicaragua; length 24.5 mm.

Page 302

whorls is similar, and of about the same size as that of
Agaroma griseoalba, although shells of A. nica are smaller.
This is the most variable of the agaronias in color. We
have seen uniform white shells and others that are black,
as well as yellow, orange, brown, gray, and intermediate
shades. Some are devoid of maculations, whereas others
are partially or entirely covered with lines, dots, or zigzags.
The aperture is dark purple in dark shells and lighter in
others. The most common color combination (represented
in the holotype) is dark gray with darker zigzags, dark
brown spiral and columellar band callus, brown proto-
conch, bluish pillar, and dark aperture. The spire whorls
are covered by callus from suture to suture.

Dimensions of holotype: length 24.7 mm, height 8.0 mm,
width 11.1 mm, spire lateral height 5.7 mm, spire base
diameter 5.8 mm; spire factor 1.017, lirae count 9.

Meristics (n = 38): Spire factor 1.01 (SD, £0.04; length
24.41 (SD, +2.82); breadth factor 0.22 (SD, +0.01); rel-
ative growth factor 1.49 (SD, +£0.07); lirae count 12.21
(SD, +1.80).

Type locality: San Juan del Sur, Rivas, Nicaragua.

Type material: Holotype, LACM 2269. Paratypes,
LACM 2270; paratypes, CAS 050208 through 050212.
Paratypes from all listed localities in Nicaragua (UCA).

Distribution: Sayulita, Nayarit, Mexico, to Puntarenas,
Costa Rica.

Referred material: MExIco: Sayulita, Nayarit (Skoglund
collection); Playa Encantada, Acapulco (Skoglund collec-
tion); Acapulco (LACM 127386), 2 specimens from Earl
Huffman collection, matching the “hypotype from Aca-
pulco” figured by BURCH & BURCH (1964:fig. 4) and ev-
idently from the same lot (J. McLean, personal commu-
nication). NICARAGUA (UCA): Jiquillo, Poneloya, Los
Playones, Masachapa, Pochomil, La Boquita, Huehuete,
Chococente, Boca de Brito, Marsella, San Juan del Sur,
La Flor, Ostional (UCA). Numerous specimens from San
Juan del Sur, Nicaragua, collected by H. N. Lowe in 1931
(Figure 19), now in LACM, San Diego Natural History
Museum, and other collections. CosTA RICA: Puntarenas,
a single specimen collected with Agaronia griseoalba by D.
Shasky, Redlands, California.

Remarks: Agaronia nica is half the size of the three larger
species (A. testacea, A. propatula, and A. griseoalba). Its
mammillate protoconch separates it from A. testacea, A.
propatula, and A. jesuitarum, as well as its low, usually
convex spire, even when the first two species are only half
grown and about the same size as fully grown A. nica.
When comparing mature A. mca with juvenile A. griseoalba
of the same color and length, the distinction lies in the low
convex spire of A. mica, its more inflated body, and its
lower lirae count. Color differences are not reliable criteria
for discrimination.

The footnote to BERRY’s (1953) description of Agaronia
murrha noted “a large series of small dark Agaronia in the

The Veliger, Vol. 30, No. 3

San Diego Museum taken in 1931 by H. N. Lowe at San
Juan del Sur, Nicaragua. These shells are mostly of pur-
plish-gray coloring with deep brown (rarely light yellow-
ish-brown) apex and fasciole, and appear to represent a
dark phase of the species here described.” The above men-
tioned specimens are typical A. nica. A true dark phase
of A. griseoalba is also now known to exist (Figures 15,
16).

This is the most common Agaronia in Nicaragua but
has not previously been recognized as a distinct species,
having been mistaken for juvenile A. testacea or A. pro-
patula. As it is common in Nicaragua, we have named it
nica, the familar name by which persons and objects from
Nicaragua are known throughout Central America.

Agaronia jesuitarum A. Lopez, Montoya
& J. Lopez, sp. nov.

(Figures 21-23)

Description: Shell small, thin, subfusiform; spire high,
straight sided, length about 22 mm, body whorl not in-
flated, lirae count relatively high, about 15. Protoconch
acuminate, caramel colored. The body whorl is grayish or
yellowish olive, profusely marked with broken zigzags or
triangles. We have also seen several specimens with an
orange ground color. The aperture is deep purple and the
inner labrum edge matches the ground color or is mottled
with purple. There is a subsutural band of slanted dashes,
similar to those of Agaronia testacea. The spire and colu-
mellar band callus is yellowish brown and covers the whorls
from suture to suture. The pillar callus pad is slightly
more raised than in other agaronias, bluish white.
Dimensions of holotype: length 21.2 mm, height 6.5 mm,
width 8.8 mm, spire lateral height 6.5 mm, spire base
diameter 5.3 mm; spire factor 1.226, lirae count 15.

Meristics (n = 38): Spire factor 1.21 (SD, £0.04), length
21.48 mm (SD, +4.68); breadth factor 0.19 (SD, +0.009);
relative growth factor 1.46 (SD, +0.06); lirae count 15.05
(SD, +1.81).

Type locality: Poneloya Beach, at river mouth, Leon,
Nicaragua.

Type material: Holotype, LACM 2271, 5 paratypes
LACM 2272, 1 paratype CAS 050213. Twenty paratypes
UCA.

Distribution: Poneloya to Boca de Brito, Nicaragua. About
40 specimens were found over the course of one year at
Poneloya in coarse sand at low tide. The first six specimens
were taken by Al and Julio Lopez in December 1982.
Four more specimens were collected at the same site a year
later, where 30 additional specimens were also found by
A. Fernandez, R. Meabe, and F. Zarrabe. Three were
found in 1984 by Michel Montoya 6 km south of Poneloya
and one at Boca de Brito, 100 km farther south. Some 20
additional specimens were found in 1985 at La Boquita
and Huehuete, and four specimens at Chococente in 1986.

A. Lopez et al., 1988

Remarks: Agaronia jesuitarum is the smallest of the Pan-
amic agaronias and also the most distinct. It is easily sep-
arated from the others based on its small size and char-
acteristic yellow or gray-olive ground color profusely
covered with small aligned spots or zigzags. Because of its
high spire and acute protoconch, it could be mistaken for
a very small, immature A. testacea; but the color, high
count of lirae, and subfusiform outline are distinctive.

This species is difficult to find. We are unable to explain
why no dead specimens have been seen. The living spec-
imens remain buried in the sand, rather than foraging on
the surface, as observed in the other species. Feeding has
not been observed. Other olivid species present at the type
locality included Agaronia griseoalba, A. nica, A. propatula,
Oliva undatella, and the ubiquitous Olivella semistriata. The
specimens of A. jesuitarum were collected by Jesuits from
the Central American University, and the name given to
the species honors their dedication.

ACKNOWLEDGMENTS

We thank Dr. James H. McLean of the Los Angeles
County Museum of Natural History, who suggested im-
provements, advised us of material in the LACM collec-
tion, edited the manuscript, and took the photographs. Dr.
Romeo Martinez, Central Agronomico Tropical de In-
vestigacion y Ensenanza (CATIE), Turrialba, Costa Rica,
helped us greatly with suggestions and techniques regard-
ing the statistics used in this study. Carol Skoglund of
Phoenix, Arizona, and David G. Robinson, Tulane Uni-
versity, made available from their collections several lots
of Agaronia used in this study. Dr. R. Kilias, Zoologisches
Museum of Humboldt-Universitat in Berlin kindly loaned
us the type specimens described by von Martens. Professor
Dr. Rudolf Fisher, Geology and Paleontology Institute,
Hannover University, West Germany, sent copies of pa-
pers by early German authors from the Senckenberg Mu-
seum, Frankfurt. Dr. Peter Sprechmann, Central Amer-
ican School of Geology, University of Costa Rica, granted
us access to the W. P. Woodring collection of papers and
documents. Lic. Teresita Aguilar, Department of Paleon-
tology, University of Costa Rica, made available to us
articles on fossil Agaronia. Professors Alejandro Cajina and
Elda Garcia, Department of Ecology, Central American
University, Managua, advised us on separating and
mounting radulae. Professor Rolando Lopez, Chairman,
Department of Ecology, Central American University, al-
lowed us the use of the instruments and laboratory in his
department. Dr. Manuel Murillo, Department of Marine
Sciences, University of Costa Rica, allowed access to the
university mollusk collection. Brother Eduardo Fernandez,
curator at the La Salle Museum of Natural History, San
José, Costa Rica, showed us the mollusk collection and
contributed some specimens. Ritha Sancho (Mrs. Michel
Montoya) collected some of the specimens used in this
study. Dr. Eugene V. Coan of Palo Alto, California, read
and commented upon the manuscript.

Page 303

LITERATURE CITED

ABBoTT, R. T. 1974. American seashells. Van Nostrand Rein-
hold: New York. 663 pp.

ABBOTT, R. T. & S. P. DANCE. 1982. Compendium of seashells.
Dutton: New York. 411 pp.

Berry, S. S. 1953. Notices of new west American marine
Mollusca. Trans. San Diego Soc. Natur. Hist. 16:405-428.

Burcu, J. Q. & R. L. Burcu. 1964. The genus Agaronia J.
E. Gray, 1928. Nautilus 77(4):110-112.

ConraD, T. A. 1849. The following new and interesting shells
are from the coasts of Lower California and Peru, and were
presented to the Academy by Dr. Thomas B. Wilson. Proc.
Acad. Natur. Sci. Phila. 4:155-156.

Fiuck, W. H. 1905. Shell collecting on the Mosquito coast of
Nicaragua—lII. Nautilus 19(2):16-19.

GMELIN, J. F. 1791. Carolia Linne Systema naturae per regna
tria naturae. Editio decima tertia. Leipzig, 1(6)(6), Vermes,
pp. 3021-3910.

Gray, J. E. 1839. Molluscous animals and their shells. Pp.
103-155. In: F. W. Beechey (ed.), The zoology of Capt.
Beechey’s voyage .. . to the Pacific and Behring’s Straits in
his Majesty’s ship Blossom. London.

HEMMEN, J. D. 1981. Olividae of Jaco, western Costa Rica.
In: D. Greifeneder (ed.), Contribution to the study of Oli-
vidae. Acta Conchiliorum of the Club Conchylia 1:128, 198-
199.

HERTLEIN, L. G. & A. M. STRONG. 1955. Marine mollusks
collected during the ‘““Askoy” Expedition to Panama, Co-
lombia, and Ecuador in 1941. Bull. Amer. Mus. Natur. Hist.
107(2):159-318.

Houprick, J. R. 1968. A survey of the littoral marine mollusks
of the Caribbean coast of Costa Rica. Veliger 11(1):4-21.

KEEN, A. M. 1958. Sea shells of tropical west America. Marine
mollusks from Lower California to Colombia. Stanford Uni-
versity Press: Stanford. 624 pp.

KEEN, A.M. 1971. Sea shells of tropical west America. Marine
mollusks from Baja California to Peru. 2nd ed. Stanford
University Press: Stanford. 1064 pp.

KILBURN, R. N. 1981. Revision of the genus Ancilla Lamarck,
1799 (Mollusca: Olividae: Ancillinae). Ann. Natal Mus.
24(2):349-463.

LaMaRCK, J. B. P. A. 1811. (Suite de la) Détermination des
especes des mollusques testacés: continuation du genre Por-
celaine et des genres Ovule, Tarriére, Ancillaire, et Olive.
Annales du Muséum d’Histoire Naturelle 16:89-114, 330-
338.

Lopez, A. 1978. Jolly olivellas, hungry agaronias. Hawaiian
Shell News 26(8):16.

MarraT, F. P. 1871. Oliva Bruguiére. /n: G. B. Sowerby (ed.),
Thesaurus conchyliorum. London. Vol. 4:1-46, pls. 342-
351.

MARTENS, E. VON. 1897. Conchologische Miscellen II. Archiv
fur Naturgesch. 63(1):157-180.

Morcu, O.A.L. 1860. Beitrage zur Molluskenfauna Central-
Amerika’s. Malakozool. Blatter 7(2):66-96.

Oxsson, A. A. 1922. The Miocene of northern Costa Rica.
Bull. Amer. Paleontol. 9(39):173-460.

Ousson, A. A. & T. L. McGinty. 1958. Recent marine mol-
lusks from the Caribbean coast of Panama with the descrip-
tion of some new genera and species. Bull. Amer. Paleontol.
39(117):1-59.

REEVE, L. A. 1850. Monograph of the genus Oliva. Concho-
logia iconica: or illustrations of the shells of molluscous
animals. London. 30 pls., text not paginated.

Rios, E.C. 1975. Brazilian marine mollusks iconography. Rio

Page 304 The Veliger, Vol. 30, No. 3

Grande, Fundacao Universidade do Rio Grande, Centro de Zone and adjoining parts of Panama. Description of Tertiary

Ciéncias do Mar, Museu Oceanografico. 331 pp. mollusks (Gastropods: Columbellidae to Volutidae). U.S.
VON MarTENS, E. 1897. Conchologische Miscellen II. Archiv Geol. Survey Prof. Paper 306-C:240-297.

fur Naturgesch. 63(11):157-180. WooprING, W. P. 1966. The Panama land bridge as a sea

WOoODRING, W. P. 1964. Geology and paleontology of Canal barrier. Proc. Amer. Phil. Soc. 110(6):425-433.

The Veliger 30(3):305-314 (January 4, 1988)

THE VELIGER
© CMS, Inc., 1988

A Review of the Generic Divisions Within the
Phyllidiidae with the Description of a New Species of
Phyllidiopsis (Nudibranchia: Phyllidiidae) from the
Pacific Coast of North America
by

TERRENCE M. GOSLINER

Department of Invertebrate Zoology and Geology, California Academy of Sciences,
Golden Gate Park, San Francisco, California 94118, U.S.A.

AND

DAVID W. BEHRENS

Pacific Gas and Electric Company, Biological Research Laboratory, P.O. Box 117,
Avila Beach, California 93424, U.S.A.

Abstract. The anatomy of Ceratophyllidia africana Eliot, 1903, and Phyllidiopsis cardinalis Bergh,
1875, the type species of their respective genera, is described. Phyllidiopsis blanca sp. nov. is described
from the Pacific coast of southern California and Baja California. It differs from other species by its
uniformly whitish coloration and low, poorly developed tubercles. Internally, it has a simple oral tube,
without associated glands. The oral tube is elongate and convoluted. The buccal and gastro-esophageal
ganglia are situated posteriorly from the circumesophageal nerve ring. The reproductive system is triaulic.
The penis is lined with several rows of conical, chitinous spines.

The present species varies in its anal position. In one specimen the anus is located below the notum,
while in the remaining five specimens it is located dorsally. Because the presence of a ventral anus is
utilized to separate Reyfria Yonow, 1986, from Phyllidia Cuvier, 1797, the status of these genera is
reviewed. The systematic position of Phyllidiopsis and Ceratophyllidia is discussed. Conflicting views of

generic distinctions within the Phyllidiidae are also discussed.

INTRODUCTION

The Phyllidiidae are a family of nudibranchs that are
characteristic of tropical, Indo-Pacific shallow-water hab-
itats. Seven species have been described from the Medi-
terranean Sea and Atlantic Ocean. These represent the
only species known outside of the Indo-Pacific. No mem-
bers of the family have been recorded from the Pacific
Ocean east of the Hawaiian Islands. The first record of a
phyllidiid from the Pacific coast of North America was
that of Phyllidia sp. (as Phellidia sp., BEHRENS, 1980). This
species is undescribed and its morphology and systematic
placement are the subject of this paper.

The generic divisions of the Phyllidiidae have been the

subject of some disagreement. Part of the problem stems
from the fact that the type species of two of the genera,
Phyllidiopsis and Ceratophyllidia, have never been com-
pletely described. This study describes the anatomy of these
species and discusses the relationships of the genera.

DESCRIPTIONS
Ceratophyllidia africana Eliot, 1903
(Figures 1A, 2)

Ceratophyllidia africana ELIOT, 1903:250.
Ceratophyllidia grisea ELIOT, 1910:436, pl. 25, figs. 3-7, syn.
nov.

Page 306

dhe Veliger) Vol 305 Noms

Figure 1

Living animals. A. Ceratophyllidia africana Eliot, 1903, Sodwana Bay National Park, South Africa, May 1981,
photo by T. Gosliner. B. Phyllidiopsis cardinalis Bergh, 1875, Middle Camp, Aldabra Atoll, March 1986, photo by
T. Gosliner. C, D. Phyllidiopsis blanca sp. nov., Islas San Benitos, August 1984, photos by Mare Chamberlin.

Distribution: This species is known only from the western
Indian Ocean, where it has been recorded from Zanzibar
(ELIoT, 1903), Coetivy Island in the Seychelles (ELIOT,
1910), South Africa (GOSLINER, 1987), and Aldabra Atoll,
Seychelles (present study).

Material: South African Museum, Cape Town, SAM A
35625, one specimen, Nine Mile Reef, Sodwana Bay Na-
tional Park, Natal, South Africa, 18-m depth, 20 May
1981, T. M. Gosliner. California Academy of Sciences,
San Francisco, one specimen, CASIZ 063262, Passe du
Bois, Aldabra Atoll, Seychelles, 10-m depth, 22 March
1986, T. M. Gosliner.

External morphology: The living animals (Figure 1A)
were 20 and 30 mm in length. The general body color was
yellowish white in the South African animal and grayish
white in the Aldabran specimen. The densely perfoliate
rhinophores were the same color as the body. The notum
bears numerous soft, spherical papillae that are attached
to the body by means of a short, slender stalk. The papillae

are readily autotomized when the animals are disturbed.
The diameter of the papillae varies from 1 to 4 mm. In
living material, the diameter of the papillae expanded and
contracted. The papillae bear black pigment spots, which
are restricted to their apical half. The anus is situated on
the dorsal surface, near the posterior end of the animal.
The lateral margins of the body, between the notum and
foot, bear approximately 90 simple gill leaflets per side.
The oral tentacles are largely separate to their bases and
have a longitudinal groove along their outer margin.

Digestive system (Figures 2A, B): Immediately posterior
to the mouth, the oral tube expands into a broad, thin-
walled vestibule. The posterior end of the vestibule nar-
rows into a thicker-walled, glandular oral tube. The oral
tube is invaginable and, in its contracted state (Figure 2B),
is contained entirely within the vestibule. The esophagus
exits at the anterior end of the oral tube. The esophagus
is elongate and highly convoluted. Also entering the oral
tube are the ducts of a pair of large oral glands. The ducts

_M.

Gosliner & D. W. Behrens, 1988 Page 307

Figure 2

Ceratophyllidia africana Eliot, 1903. A. Digestive system retracted: bg, buccal ganglia; e, esophagus; ge, gastro-
esophageal ganglia; gs, glandular segment of esophagus; og, oral glands; ot, oral tube; rm, retractor muscle; ve,
vestibule. B. Digestive system everted, lettering same as A. C. Reproductive system: am, ampulla; bc, bursa copulatrix;
fgm, female gland mass; p, penis; pr, prostate; rs, receptaculum seminis; ud, uterine duct; va, vagina; vd, vas deferens.

Page 308

of these glands terminate at the anterior end of the oral
tube, adjacent to the esophagus. Posteriorly, the esophagus
expands into a short glandular segment prior to its entrance
into the thin-walled stomach within the digestive gland.

Central nervous system: The ganglia forming the circum-
esophageal nerve ring are highly cephalized, with complete
fusion of the cerebral and pleural ganglia. The cerebro-
pleural ganglia are appressed to each other, without a
distinct commissure. The pedal ganglia are separated by
a short commissure. The buccal and gastro-esophageal
ganglia are attached to the circumesophageal nerve by long
connectives. When the oral tube is completely invaginated
within the vestibule these ganglia are situated immediately
ventral to the circumesophageal nerve ring.

Reproductive system (Figure 2C): The arrangement of
organs is triaulic. The ampulla is short and saccate, nar-
rowing abruptly near its division into the oviduct and vas
deferens. The oviduct is short and enters the female gland
mass near the albumen gland. The uterine duct emerges
from the female gland mass and joins the duct of the pear-
shaped receptaculum seminis. The spherical bursa copu-
latrix is thin-walled and black in both specimens examined.
It has an elongate duct and joins the duct of the receptac-
ulum and continues proximally to the vaginal opening,
adjacent to the penis. The vas deferens is prostatic distally
and narrows into a muscular, ejaculatory segment. The
proximal portion is devoid of any chitinous spines.

Discussion: Ceratophyllidia africana Eliot, 1903, was de-
scribed from a single specimen collected from Zanzibar.
Exior (1910) later described C. grisea from a single spec-
imen collected in the Seychelles. He stated that C. grisea
differed from C’ africana in its gray rather than yellowish
color and by having larger papillae that obscured most of
the notum. No additional records of these species appeared
until GOSLINER (1987) reported C. africana from Natal,
South Africa. This specimen, examined in the present
study, was yellowish in color, but had large, dense papillae
as described for C. grisea. The specimen collected at Al-
dabra was grayish in color with sparser papillae. In both
living specimens, it was noted that the diameter of the
papillae could be altered by expansion or contraction. Dis-
section of these specimens demonstrated no internal dif-
ferences between them, except in the state of contraction
of the buccal apparatus. Therefore, C. grisea is here re-
garded as a junior subjective synonym of C. africana.

Phyllidiopsis cardinalis Bergh, 1875
(Figures 1B, 3)
Phyllidiopsis cardinalis BERGH, 1875:670, pl. 16, figs. 11-15.

Distribution: This species is known throughout the Indo-
Pacific tropics, from Aldabra Atoll to the Hawaiian Islands
(present study).

The Veliger, Vol. 30, No. 3

Material: California Academy of Sciences, San Francisco,
CASIZ 063263, one specimen, Poipu Beach Park, Kauai,
Hawaiian Islands, under rock, intertidal zone, 16 Feb-
ruary 1986, Michael Gosliner. CASIZ 063264, one spec-
imen, Poipu Beach Park, Kauai, Hawaiian Islands, under
rocks, intertidal zone, 19 February 1986, Michael Gos-
liner. CASIZ 063265, one specimen, Passe Houreau, off
Middle Camp, Aldabra Atoll, Seychelles, 2-m depth, 18
March 1986, T. M. Gosliner.

External morphology: The living animals (Figure 1B)
were 12-24 mm long. The color is complex. The foot, anal
papilla, rhinophores, and notum are yellowish. This pig-
ment is overlain with papillae that are dark brown mar-
ginally, lighter brown to cream more medially. The spaces
between papillae are off-white to mustard yellow. The
raised central portion is finely papillate, off-white to cream.
Three central raised portions on this ridge are dirty brown.
The rhinophores are densely perfoliate. The lateral mar-
gins between the notum and foot bear numerous, simple,
leaflike gill lamellae. The tubercles covering the dorsum
are composed of several small rounded tubercles. The anus
is situated medially on the dorsum near the posterior end
of the body. There are approximately 110 leaflets per side.
The oral tentacles are united for their entire length and
possess a groove along both lateral margins.

Digestive system (Figure 3A): The most anterior portion
of the oral tube is rugose and glandular. More posteriorly,
it is smooth and curves anteriorly. Slightly more anteriorly
to this point, the oral tube narrows into the esophagus. A
retractor muscle inserts into either side of the oral tube at
its junction with the esophagus. The esophagus is elongate
and convoluted, passing through the circumesophageal nerve
ring. Near its posterior limit the esophagus expands slight-
ly to a segment that contains circular muscle fibers. Pos-
terior to this it curves and enters the stomach within the
digestive gland.

Central nervous system: The ganglia of the circum-
esophageal nerve ring are highly concentrated. The cere-
bral and pleural ganglia are almost entirely fused. The
cerebro-pleural ganglia are appressed to each other, with-
out a distinct, narrowed commissure. The pedal ganglia
are separated by a short commissure. The paired buccal
and gastro-intestinal ganglia are situated posteriorly, im-
mediately anterior to the muscular portion of the esophagus
(Figure 3A).

Reproductive system (Figure 3B): The saccate ampulla
narrows abruptly into the postampullary duct, prior to its
division into the oviduct and vas deferens. The oviduct is
short and enters the distal portion of the female gland
mass. The elongate uterine duct emerges from the female
gland mass and joins the pyriform receptaculum seminis
at the duct that joins the receptaculum with the spherical
bursa copulatrix. From the bursa copulatrix the elongate
vaginal duct runs proximally to a joint gonopore with the

T. M. Gosliner & D. W. Behrens, 1988

Page 309

Figure 3

Phyllidiopsis cardinalis Bergh, 1875. A. Digestive system: bg, buccal ganglia; cns, central nervous system; e, esophagus;
ge, gastro-esophageal ganglia; ms, muscular segment of esophagus; ot, oral tube; rm, retractor muscles. B. Repro-
ductive system: am, ampulla; bc, bursa copulatrix; fgm, female gland mass; p, penis; pr, prostate; rs, receptaculum

seminis; ud, uterine duct; va, vagina; vd, vas deferens.

penis. The vas deferens is prostatic distally and widens
into a muscular portion. There are no cuticular spines
associated with the penis.

Discussion: Phyllidiopsis cardinalis Bergh, 1875, is the type
species of the genus. Some aspects of its morphology were
described in the original description, but details of the
reproductive anatomy were not examined. The digestive
system is characterized by a short muscular segment at the
posterior end of the esophagus. As far as is known, this is
the only member of the genus to have this structure. Another
species, P. tuberculata Risbec, 1928, is similar to the present
species in that it also has compound tubercles and has
similar coloration. As suggested by PRUVOT-FOL (1957),
this species is probably synonymous with P. cardinalis. In
RIsBEC’s (1928) description of this species, he indicates
that a large salivary gland is present. This is likely the
blood gland rather than a salivary gland.

Phyllidiopsis blanca Gosliner & Behrens, sp. nov.
(Figures 1C, D, 4, 5)

Phellidia (sic) sp.: BEHRENS, 1980:100, fig. 144.
Phyllidia sp.: BEHRENS & GATEWOOD, 1986:139.

Type material: Holotype, California Academy of Sci-
ences, San Francisco, CASIZ 063266, San Nicolas Island,
¥; mi (1.2 km) S of Sand Spit Light, 33°12’N, 120°25’W,
CIRP Station SNI-2, 40 ft (13 m) deep, 22 October 1982,
Jack Engle, 25 mm preserved. Paratypes, CASIZ 063267,
5 specimens, Isla San Benitos, 28°20’N, 115°40’W, 11 m
deep, 6 August 1984, Jim Gatewood and Marc Cham-
berlin.

Distribution: Pacific coast of California and Baja Cali-
fornia, Mexico, from Santa Barbara Island to Isla San
Benitos. Specimens examined in this study were collected
from San Nicolas Island and Isla San Benitos. Photographs
of specimens made available to us indicate that this species
occurs at least as far north as Santa Barbara Island and
from several localities within this range.

External morphology: The living animals (Figures 1C,
D, 4A) are 10-25 mm long. The general body color is
white to grayish white. The sparsely perfoliate rhino-
phores are the same color as the body. The notum bears
numerous soft, low tubercles. Although varying in diam-
eter, these tubercles are more or less evenly dispersed over
the notal surface. No gradation in size occurs as the tu-
bercles near the notal margin. In five of the six specimens

Page 310

The Veliger, Vol. 30, No. 3

TK

{/c))

{

Figure 4

Phyllidiopsis blanca sp. nov. A. Dorsal view of living animal. B. Ventral view of preserved specimen with ventral
anus: an, anus; f, foot; ga, genital apertures; gi, gills; h, head. C. Section of gills. D. Schematic view of gills, showing

alternation of large and small gill filaments.

examined, the anus was located dorsally, near the posterior
end of the animal. In the sixth specimen (Figure 4B) from
Islas San Benitos, the anus is located posteroventrally on
the hyponotum. The gills are arranged laterally, between
the notum and foot. It is difficult to establish the exact
number of gill leaflets, as the gill is a series of large lamellae
irregularly interdigitated by smaller gill leaflets (Figures

4C, D). A count of the major gill elements in the holotype
indicates that they may not be bilaterally equal, with the
left side bearing about 70 leaflets and the right side ap-
proximately 60. This is due to the interruption of the
leaflets on the right side, in the vicinity of the gonopores.
Remnants of oral tentacles are present as grooves along
either side of the flattened, quadrangular head.

T. M. Gosliner & D. W. Behrens, 1988 Page 311

Figure 5

Phyllidiopsis blanca sp. nov. A. Digestive system with central nervous system: a, anus; cns, central nervous system;
i, intestine. B. Detail of digestive system with central nervous system removed: bg, buccal ganglia; e, esophagus;
ge, gastro-esophageal ganglia; gs, glandular segment of esophagus; ot, oral tube. C. Reproductive system: am,
ampulla; be, bursa copulatrix; fgm, female gland mass; p, penis; pr, prostate; rs, receptaculum seminis; ud, uterine
duct; va, vagina; vd, vas deferens. D. Penial armature.

Page 312

Digestive system (Figures 5A, B): The oral tube is nar-
rowest at the mouth, gradually widening posteriorly. The
oral tube is simple throughout its length and is devoid of
associated oral glands. It recurves anteriorly and narrows
abruptly into the esophagus. The esophagus consists of
several convolutions, which traverse the length of the oral
tube. Near its posterior limit, the esophagus expands into
a glandular segment, curves anteriorly, and enters the
digestive gland. More posteriorly, the intestine emerges
again from the digestive gland and continues posteriorly
to its termination at the anus.

Central nervous system: The ganglia constituting the
circumesophageal nerve ring are highly concentrated. The
paired cerebral and pleural ganglia are largely fused. The
cerebral ganglia are appressed to each other, without a
distinctly narrowed commissure. The pedal ganglia are
separated by a short commissure. Extending posteriorly
from the cerebro-pleural ganglia are the elongate buccal
nerves. They are joined to the paired buccal ganglia along
the sides of the esophagus. Immediately posterior to the
buccal ganglia are the gastro-esophageal ganglia. In one
specimen the buccal and gastro-esophageal ganglia are
situated near the posteriormost loop of the esophagus. In
a second specimen, they are situated even more posteriorly,
just anterior to the glandular swelling of the esophagus.

Reproductive system (Figure 5C): The reproductive sys-
tem is triaulic. The ampulla is short and saccate. Proxi-
mally, it narrows into the postampullary duct just prior
to its bifurcation into the oviduct and vas deferens. The
oviduct enters the female gland mass after a short distance.
The various nidamental glands that constitute the female
gland mass cannot be differentiated, owing to poor pres-
ervation. The uterine duct emerges from the female gland
mass near its juncture with the oviduct. It joins the recep-
taculum seminis and bursa copulatrix at their common
base. The receptaculum has a short duct while the bursa
is inserted directly on to the uterine duct. Emerging from
the proximal end of the juncture of the uterine duct, re-
ceptaculum, and bursa, is the vaginal duct. It is elongate
and widens gradually towards the gonopore. The vas def-
erens is prostatic distally following its separation from the
oviduct at the proximal terminus of the postampullary
duct. It narrows into a muscular ejaculatory segment that
terminates adjacent to the vaginal and nidamental open-
ings. The proximal end of the ejaculatory segment (Figure
5D) contains 4 or 5 rows of sharp, chitinous spines, with
approximately 12 spines per row.

Discussion: Phyllidiopsis blanca is placed in Phyllidiopsis
because it lacks a ring of oral glands present in Phyllidia
and Reyfria. The presence of a ventral anus in one specimen
of P. blanca represents an acquisition of this character
independently from that of Reyfria.

The known morphology of species of Phyllidiopsis is
compared in Table 1. Phyllidiopsis blanca and P. berghi
Vayssiére, 1902, are the only known species within the

The Veliger, Vol. 30, No. 3

family that have uniformly whitish coloration. All other
species have complex color patterns and, with the excep-
tions of P. cardinalis and P. tuberculata, possess some black
pigment on the notum. Phyllidiopsis berghi differs from P.
blanca in having a distinct vestibule at the anterior end
of the oral tube and a much longer oral tube (BOUCHET,
1977:fig. 17). Phyllidiopsis blanca is also similar to P.
gynenopla Bouchet, 1977, in its arrangement of the diges-
tive system, but lacks the distinct armature surrounding
the nidamental opening of the female reproductive system.

DISCUSSION OF GENERA

The distinctions between genera within the Phyllidiidae
have been discussed by several workers (BERGH, 1875,
1889; PRuvoT-FOoL, 1956, 1957; Marcus & Marcus,
1962; EDMUNDS, 1972; WAGELE, 1985; YONOw, 1986).
The major characteristics utilized to separate genera are
the elaboration of the oral tube and associated glands, the
position of the anus, and the elaboration of the oral ten-
tacles.

Most studies have differentiated Phyllidia and Reyfria
(as Fryeria) from Phyllidiopsis and Ceratophyllidia on the
basis of the possession of a large mass of oral glands sur-
rounding the oral tube in the former two genera.

In Phyllidiopsis and Ceratophyllidia the arrangement of
oral glands, when present, is more complex. The type
species of Phyllidiopsis, P. cardinalis Bergh, 1875, and most
other members of the genus lack oral glands (Table 1), as
in P. blanca. Phyllidiopsis papilligera Bergh, 1890 (Marcus
& Marcus, 1962:fig. 24) and P. molaensis have a single
nodular oral gland, which enters the posterior end of the
oral tube. In P. papilligera there is a caecum at the distal
end of the gland that is absent in P. molaensis. Phyllidiopsis
tuberculata (RISBEC, 1928) was reported to have a large
oral gland, but PRUVOT-FOL (1957) has suggested that this
is actually the blood gland. There is some question as to
whether P. tuberculata may actually be a junior synonym
of P. cardinalis Bergh, 1875. Both species have compound
tubercles and are similar in their coloration. Ceratophyllidia
africana has a pair of large oral glands with ducts entering
the oral tube and running its length adjacent to the esoph-
agus (ELIOT, 1903; present study).

Phyllidia has also been characterized by having well
developed retractor muscles, while they are apparently
absent in Phyllidiopsis (PRUVOT-FOL, 1957). On the basis
of lacking retractor muscles, EDMUNDS (1972) placed a
phyllidiid species in Phyllidiopsis, despite the fact that it
had prominent oral glands surrounding the oral tube. Sim-
ilarly, Ceratophyllidia africana has large retractor muscles
but lacks a ring of distinct glands. Thus, the presence of
both a mass of oral glands and retractor muscles cannot
be used to separate Phyllidia from Phyllidiopsis and Cer-
atophyllidia. It seems that the mass of oral glands in Phyl-
lidia and Reyfria is far more likely to represent a unique
derivation within the Phyllidiidae, and should be afforded
greater weight in differentiating these genera from Phyl-

Page 313

T. M. Gosliner & D. W. Behrens, 1988

Apnis juasaid

LL6| ‘LAaHONO|g

688] HOwdg

LS6Il “1O.J-LOANUg

LS6] “1OJ-LOANAg

LL6| ‘LaHONOg
‘TO6L “AUDISSAVA,

LLOI “YIATN
Z9G6] ‘SNOUVIT
2 SNOAVI
‘0681 ‘HOWdg
LS6| ‘1lOq-LOA
-NUd 876] ‘OAASTY
Apnjs juasoid
‘LS6] ‘1OJ-LOANUg

SIIDUIIIJIY

powe

powe

powueun

suajajap
StA

snosouwnu

apis
Jad 08-0

ayesuoya

a1esu0ja

a1esu0ja

SUL dAJOU

0} s0119]Ue pa

-jenIs spurs [eo
-onq YIM a}esuoya

ayesuoya

a}esuoja

a}eSu0]a

JATIOIUUOD
yesonq-o1qa.ar)

juasqe

juasqe

é quasaid

juasqe

juasqe

juasqe
jesiop
juasaud

esusa
yuasaid

¢ JUesqe

juasqe

spurs
[e140

21hq
-1]S9A OU

aynq

-1)S9A OU
2[nq

-1]S9A OU
2[nq
-1]S9A 19

“yoru yam

aqnq
-1]S9A OU
aqnq
-1]S9A JO
PAPE YER E
aynq
-1]S9A Yoru

aynq
BSS GH
apnqusaa
aBie] YIM
2[nq
-1]S9A OU

aqni [R19

jnoysnoiy}
pouun
paitun Ajasey

ajyeredas 410ys

paqun

payun Ajasse]

aseq

ye paqrun ‘joys
ayed

-edas ‘jeoru09

pesny
Ajasie] ‘punos

pasny Ajasue]

sopor}ual [PIO

‘sisdowpyypdyg jo Ayyiqeisiea jeosojoydso0py

CLAS

puno
‘g,durts
jeotuayds
oY
‘g{durts
peoru0s
‘ajduuts

punoduro09
puno.
‘g,durts
puno.
‘gjduuts
Jeotuos
‘g,duits

SIEM
Moy ‘a]durts

punodwo

punoduwio09

saposaqn [,

onuepy “q

onueny “

puryrey

WRN ITA,

onueny “J
ewueued jo
JSBOD INURNY

OnURTY “M

elu

-opayet) MON
DOL DEA

uonnqinstq

‘aou “ds poun)q

LL61 yYyonog
pj) qouauks

6881
‘YyBIIg vIDIL]S

LS61 [04-104

nig quay *

LS61 [Oq-104

“nig vypuwuas

COG] 24QIS
-skv A 1ys1aq
LL61 49

-AdJN Sisuavjou

0681 “Yo19g

viasypidod *

(8261 ‘99qsty)

DyDjNIL4aqn}

9281 ‘Ysi9g

SU]DUIPLDI

d

d

d

d

d

d

d

Page 314

lidiopsis and Ceratophyllidia. Hence, EDMUNDS’ (1972)
species should be placed in Phyllidia.

The systematic position of Ceratophyllidia has been the
subject of confusion. Since its original description (ELIOT,
1903), most workers have considered Ceratophyllidia as a
junior synonym of Phyllidiopsis (THIELE, 1931; PRU-
voT-FOL, 1957; FRANC, 1968). Marcus & Marcus (1962)
suggested that Ceratophyllidia should be regarded as a dis-
tinct genus on the basis of its possession of stalked papillae.
Unfortunately, the opinions regarding its generic status
were based solely on ELIOT’s incomplete descriptions (1903,
1910). Examination of the present material provides a
more complete basis of comparison. The fleshy, stalked,
readily detachable papillae are unique to Ceratophyllidia.
Also the presence of paired oral glands with ducts running
parallel to the esophagus within the oral tube is known
only from Ceratophyllidia. This additional fact lends sup-
port to the contention that Ceratophyllidia represents a
distinct genus.

The systematic position of Fryeria Gray, 1853, had never
been in question. Recently, however, YONOW (1986) cor-
rectly pointed out that the name Fryeria had been incor-
rectly applied to F. ruppelli rather than to Phyllidia pus-
tulosa Cuvier, 1804. She considered Fryeria as a junior
synonym of Phyllidia, because P. pustulosa has a dorsal
anus, and substituted the Reyfria for the species with a
ventral anus. The fact that specimens of Phyllidopsis blanca
examined in this study are variable in the position of the
anus (dorsal in five specimens, ventral in one) casts serious
doubts as to whether Rey/fria should be separated from
Phyllidia. Certainly, the degree of intraspecific variability
of this character within the Phyllidiidae must be examined
in greater detail.

ELIOT (1903) stated that, although it was not possible
to examine the vas deferens of Ceratophyllidia africana, it
was likely that it was armed with hooks, as in other mem-
bers of the family. THIELE (1931) also characterized the
family as having spines within the male duct. However,
WAGELE (1985) observed that the male duct of Phyllidia
pulitzerr lacked armature. Similarly, the type species of
Phyllidiopsis and Ceratophyllidia also lack any armature
(present study). It appears that this character varies within
genera.

ACKNOWLEDGMENTS

We thank Jim Gatewood, Mare Chamberlain, and Jack
Engle for kindly providing us with specimens of Phyllid-
topsis blanca. Marc Chamberlain also graciously permitted
us to use his photographs of this species. We also thank
Marc Charnow of the California Academy of Sciences for
printing the final photographic prints of the living animals.

The Veliger, Vol. 30, No. 3

LITERATURE CITED

BEHRENS, D. 1980. Pacific nudibranchs. A guide to the opis-
thobranchs of the northeastern Pacific. Sea Challengers: Los
Osos, California. 112 pp.

BEHRENS, D. & J. GATEWOOD. 1986. New opisthobranch rec-
ords for the west coast of Baja California Shells and Sea
Life 18(9):139-142.

BERGH, R. 1875. Neue Bietrage zur Kenntniss der Phyllidi-
aden. Verh. der k. k. zool-bot Gesell. Wien 25:659-674.
BERGH, R. 1889. Malacologische Untersuchungen, 3, Nudi-
branchien vom Meere der Insel Maritius. Jn: C. Semper
(ed.), Reisen im Archipel der Philippinen. Wiss. Res. 2, 3

(16) pt. 2:815-872.

BERGH, R. 1890. Report on the nudibranchs. Report on the
results of dredging, under the supervision of Alexander Agas-
siz, in the Gulf of Mexico (1877-1878) and in the Caribbean
Sea (1879-1880), by the U.S. Coast Survey steamer “Blake,”
Lieut. Commander C. D. Sigsbee, U.S.N. and Commander
J. R. Bartlett, U.S.N. commanding. Bull. Mus. Comp. Zool.
Harv. 19:155-181.

BoucHET, P. 1977. Opisthobranches de profondeur de l’océan
atlantique: II—Notaspidea et Nudibranchiata. Jour. Moll.
Stud. 43:28-66.

Epmunpbs, M. 1972. Opisthobranchiate Mollusca from the
Seychelles, Tanzania and the Congo, now in the Tervuren
Museum. Rey. Zool. Bot. Afr. 85:67-92.

Euiot, C. 1903. On some nudibranchs from East Africa and
Zanzibar. II. Proc. Zool. Soc. Lond. 1903(1):250-257.
EuiotT, C. 1910. Nudibranchs collected by Mr. Stanley Gar-
diner from the Indian Ocean in H.M.S. Sealark. Trans.

Linn. Soc. Lond. 13:411-438.

FRANC, A. 1968. Sous-classe de opisthobranches. Jn: P. Grassé
(ed.), Traité de Zoologie, 5 (3), Mollusques Gasteropodes
er Scaphopodes. Masson et Cie: Paris.

GOSLINER, T. 1987. Nudibranchs of southern Africa. A guide
to opisthobranch molluscs of southern Africa. Sea Chal-
lengers: Monterey, California.

Marcus, Ev. & Er. Marcus. 1962. Opisthobranchs from
Florida and the Virgin Islands. Bull. Mar. Sci. 12(3):450-
488.

MEYER, K. 1977. Dorid nudibranchs of the Caribbean coast
of the Panama Canal Zone. Bull. Mar. Sci. 27(2):299-307.

PruvoT-FoL, A. 1956. Revision de la famille des Phyllidiadae.
1. Jour. Conchyl. 96:55-80.

PRUVOT-FOL, A. 1957. Revision de la famille des Phyllidiadae.
2. Jour. Conchyl. 97:104-135.

RIsBEC, J. 1928. Contribution a l’étude des nudibranches Néo-
Calédoniens. Faune Colon. Frangaise 2(1):1-328.

THIELE, J. 1931. Handbuch der Systematischen Weichter-
kunde. 1. Gustav Fischer: Jena.

VAYSSIERE, A. 1902. Opisthobranches. Pp. 221-270. In: Ex-
péditions scientifiques du ““Travailleur” et du “Talisman”
pendant les annees 1880-1883. Ouvrage publie sous les aus-
pices du ministre de l’instuction publique, Paris.

WAGELE, H. 1985. The anatomy and histology of Phyllidia
pulitzeri Pruvot-Fol, 1962, with remarks on the three Med-
iterranean species of Phyllidia (Nudibranchia, Doridacea).
Veliger 28(1):63-79.

Yonow, N. 1986. Red Sea Phyllidiidae (Mollusca, Nudibran-
chia), with descriptions of new species. Jour. Natur. Hist.
20:1401-1428.

The Veliger 30(3):315-318 (January 4, 1988)

THE VELIGER
© CMS, Inc., 1988

A New Species of Gastropteron

(Gastropoda: Opisthobranchia) from

Reunion Island, Indian Ocean

TERRENCE M. GOSLINER

Department of Invertebrate Zoology and Geology, California Academy of Sciences,
Golden Gate Park, San Francisco, California 94118, U.S.A.

GARY C. WILLIAMS

Department of Marine Biology, South African Museum, P.O. Box 61,
Cape Town 8000, South Africa

Abstract. Gastropteron michaeli sp. nov. is described from Reunion Island. Aspects of its external
and internal morphology clearly differentiate this species from other members of the genus.

INTRODUCTION

During the course of a collecting expedition to Reunion
Island in the western Indian Ocean in July 1977, one of
us (G.C.W.) and Michael Gosliner collected 16 species of
opisthobranch gastropods. Included in this collection is an
undescribed species of Gastropteron. This paper describes
the morphology of this species and compares it with closely
allied congeners.

METHODS

Penial morphology was determined by clearing and stain-
ing of the material. The whole penis was stained in a dilute
solution of 70% EtOH and acid fuchsin for 1 min. It was
then dehydrated in a series of three alcohols (80%, 95%,
100% EtOH, for 1 min each). The specimen was then
cleared in xylene for 2 min and mounted in Permount on
a microscope slide.

DESCRIPTION
Family GASTROPTERIDAE Swainson, 1840
Gastropteron Meckel (in Kosse), 1813
Gastropteron michaeli Gosliner & Williams, sp. nov.
(Figures 1, 2)

Type material: Holotype, California Academy of Sci-
ences, San Francisco, CASIZ 063270, 2 km S of St. Giles,

Reunion Island, Indian Ocean, under rocks on dead coral
reef, 2m depth, 28 July 1977, Michael L. Gosliner. Para-
type, one specimen, CASIZ 063271, 2 km S of St. Giles,
Reunion Island, under rocks on dead coral reef, 2 m depth,
28 July 1977, M. L. Gosliner.

Etymology: This species is named after Michael L. Gos-
liner. He has been an enthusiastic collector and supporter
of our research efforts. He collected both of the specimens
of this species.

External morphology: The living animals (Figure 1) were
3-5 mm in length. The body was uniformly yellow-orange
with large maroon-brown spots scattered over the surface
of the head shield, posterior shield, and dorsal and ventral
surfaces of the foot.

The head shield is roughly triangular in shape, broadest
anteriorly. Its posterior end is involuted to form a siphon
with a thin, cylindrical medial crest. The parapodia are
thin and low, barely extending on to the dorsal surface of
the animal. The posterior shield is ovoid and elongate,
without a flagellum or auxiliary appendages. The foot is
not distinctly separated from the parapodia. When the
animal is actively crawling, the foot is extended well behind
the posterior end of the visceral hump. A distinct pedal
gland was not observed on the ventral side of the foot, but
this may be a result of preservation. The simply plicate

Page 316

The Veliger, Vol. 30, No. 3

Figure 1

Gastropteron michaeli sp. nov., living animal.

ctenidium is poorly developed, consisting of 3 or 4 simple
leaflets. The anus is located immediately posterior to the
ctenidium. The genital aperture is situated anterior to the
ctenidium. From it, the sperm groove runs anteriorly to
the male genital aperture on the right side of the head.
Owing to fixation of the material in Bouin’s solution, the
shell, if present, was dissolved.

Digestive system: The buccal mass is muscular through-
out its length. From the posterior end of the buccal mass,
emerges the narrow esophagus. It expands into a short,
thin-walled crop, which approximates the buccal mass in
size. The crop is devoid of chitinous plates or folds. It
narrows again posteriorly, where a short esophageal por-
tion enters the digestive gland. The intestine emerges from
the digestive gland, curves posteriorly, and emerges at the
anus, posterior to the gill.

Within the buccal mass the jaws are poorly developed,
devoid of distinct chitinous rodlets, and reduced to a thin
cuticular lining. The radular formula is 21-22 x 3.1.0.1.3.
in the two specimens examined. The inner lateral tooth
(Figure 2A) is broad with an elongate cusp and a broad
base. The masticatory border of the tooth may be entirely
smooth or with up to five irregular denticles along its
margin. The presence or absence of denticles varies within

the radula of a single individual. The outer laterals are
narrow with a broader base. They are devoid of denticles.

Central nervous system (Figure 2B): The arrangement
of ganglia is euthyneurous and highly cephalized, with a
short visceral loop. The cerebral ganglia are large and
appressed to each other. Large nerve thickenings emerge
from the anterior and lateral sides of each cerebral gan-
glion. The pedal ganglia are as large as the cerebrals, and
are separated from each other by a short, narrow com-
missure. The left pleural ganglion is separated from the
left cerebral and pedal ganglia by a short connective. Im-
mediately posterior and appressed to the left pleural is the
subintestinal ganglion. The larger visceral ganglion is di-
rectly behind the subintestinal ganglion. Emanating from
the posterior end of the visceral ganglion are three nerves.
The innermost of these is the visceral loop. The short
visceral loop joins the posterior end of the supraintestinal
ganglion adjacent to the osphradial nerve. The suprain-
testinal ganglion is partially fused with the right pleural
ganglion.

Reproductive system (Figure 2C): The system is mon-
aulic. The ovotestis consists of numerous round bodies.
The ampulla is narrow and winding. It narrows further
proximally and winds around the outer surface of the

T. M. Gosliner & G. C. Williams, 1988

Page 317

Figure 2

Gastropteron michaeli sp. nov. A. Radular teeth, showing variation in inner lateral tooth and outer laterals, scale =
20 um. B. Central nervous system. Key: c, cerebral ganglion; e, eye; on, osphradial nerve; pe, pedal ganglion; pl,
pleural ganglion; sb, subintestinal ganglion; sp, supraintestinal ganglion; v, visceral ganglion; scale = 250 um. C.
Reproductive system. Key: am, ampulla; bc, bursa copulatrix; fgm, female gland mass; ga, genital atrium; ot,
ovotestis; rs, receptaculum seminis; scale = 1.0 mm. D. Penis. Key: mb, muscular bulb with chitinous spines; p,

penial papilla; pr, prostate; scale = 0.5 mm.

female gland mass. Near the middle of the hermaphroditic
duct, a short duct leds to the pyriform receptaculum sem-
inis. The hermaphroditic duct curves proximally and ter-
minates at the common genital atrium. The spherical, thin-
walled bursa copulatrix has a narrow, elongate duct, which
also joins the common genital atrium near the gonopore.
The female glands could not be differentiated from one
another in the fully dissected specimen.

The penis (Figure 2D) is well developed and complex
in its structure. The prostate is bilobed, with one of the
lobes significantly thicker than the other. The two lobes
are united for their proximal one-third. From the proximal
end of the prostate, a narrow duct emerges and enters the
small, conical penial papilla. A curved fleshy, papilla is
situated more proximally, within the penial sac. The larg-
est portion of the prostate enters a bulbous, muscular sec-

tion. Within this muscular region are four rows of curved,
chitinous spines. The left lobe has four spines, the poste-
riormost three, the middle lobe seven, and the anteriormost
four. The anterior end of the muscular portion joins the
penial sac anteriorly. The penial sac is thin and elongate,
terminating at the male gonopore.

DISCUSSION

In a recent review of the genus, GOSLINER (1984) listed
15 described species of Gastropteron. Since then, one ad-
ditional species, G. vespertilium Gosliner & Armes, 1984,
has been described. Of these 16 species, only six are known
to lack a flagellum or other auxiliary process on the pos-
terior shield. Gastropteron brunneomarginatum Carlson &
Hoff, 1974, was recorded as lacking a flagellum. However,

Page 318

examination of specimens of this species from New Guinea
(present study) indicates that a flagellum may be present
or absent in individuals from a single population.

Of the species that always lack a flagellum, only Gas-
tropteron flavobrunneum and G. michaeli are yellowish
with brown spots (GOSLINER, 1984). Gastropteron flavo-
brunneum is lighter in color and lacks any orange pigment.
The radula of G. flavobrunneum has six or seven teeth per
half row, while in G. michaeli there is a maximum of four
teeth per half row. The inner lateral teeth of G. flavo-
brunneum lack any denticles on the masticatory border,
while in G. michaeli denticles may be present or absent.
The penial morphology of the two species differs markedly.
The penis of G. flavobrunneum has a distinct spermatic
bulb, in addition to the single prostate, and the peniai
papilla has a discoidal apex. In G. michaeli the prostate
is bilobed, there is a muscular region with chitinous spines,
and the penial papilla is conical.

The penial morphology has been described for only six
of the 16 known species. It varies considerably between
species. Of the described species, only Gastropteron ladrones
Carlson & Hoff, 1974, is similar to that of G. michaeli
in having a muscular region with cuticular spines and a
separate duct leading to the penial papilla (GOSLINER, in
press). At least one other undescribed Indo-Pacific Gas-

The Veliger, Vol. 30, No. 3

tropteron species has a similar penial morphology. It ap-
pears that further examination of this character, by stain-
ing and clearing of preparations, will provide information
useful in establishing natural groupings of species within
the Gastropteridae.

ACKNOWLEDGMENTS

We thank Bill Liltved for preparing the final figures, with
the exception of the living animal, and Michael Gosliner
for collecting the specimens.

LITERATURE CITED

CARLSON, C. & P. Horr. 1974. The Gastropteridae of Guam,
with descriptions of four new species (Opisthobranchia:
Cephalaspidea). Publ. Seto Mar. Biol. Lab. 21(5/6):345-
363.

GOSLINER, T. 1984. Two new species of Gastropteron (Gastrop-
oda: Opisthobranchia) from southern Africa. Publ. Seto Mar.
Biol. Lab. 29(4/6):231-247.

GOSLINER, T. In press. The Philinacea (Gastropoda: Opis-
thobranchia) of Aldabra Atoll, with descriptions of five new
species and a new genus. Proc. Biol. Soc. Wash.

GOSLINER, T. & P. ARMES. 1984. A new species of Gastropteron
from Florida (Gastropoda: Opisthobranchia). Veliger 27(1):
54-64.

The Veliger 30(3):319-324 (January 4, 1988)

THE VELIGER
© CMS, Inc., 1988

pHieshinsmiNeconduol veo! yeerciia WwW errlly 188i trom the

Pacific, with the Description of a New Species

DAVID W. BEHRENS

Biological Laboratory, Pacific Gas and Electric Company, P.O. Box 117,
Avila Beach, California 93424, U.S.A.

TERRENCE M. GOSLINER

Department of Invertebrate Zoology and Geology, California Academy of Sciences,
Golden Gate Park, San Francisco, California 94118, U.S.A.

Abstract.

A new species of Polycerella, P. glandulosa is described from the Pacific coast of California

and the Gulf of California. It differs from the Atlantic P. emertoni, the only other member of the genus,
in several aspects of its external and internal morphology. Polycerella glandulosa is characterized by its
few rhinophoral lamellae and its compoundly digitate extra-branchial appendages.

INTRODUCTION

Specimens of an undescribed Polycerella were abundant
along the California coast from Morro Bay to San Diego,
in late 1982 and throughout 1983. Specimens have also
been collected commonly at various localities within the
Gulf of California. This paper describes the morphology
and aspects of the biology of this species and compares
them to the only other known member of the genus, Poly-
cerella emertoni Verrill, 1881.

Polycerella glandulosa Behrens & Gosliner, sp. nov.
(Figures 1-4)

Type material: Holotype: California Academy of Sci-
ences, San Francisco, CASIZ 063272, one 7 mm specimen,
Punta Gringa, Bahia de los Angeles, Baja California,
Mexico, 10 m depth, 1 October 1984, T. M. Gosliner.
Paratypes: CASIZ 063273, four specimens, Punta Gringa,
10 m depth, 1 October, 1984, T. M. Gosliner; CASIZ
063268, 8 specimens, Los Islotes, north of La Paz, Baja
California Sur, Mexico, 15-20 m depth, 22 July 1985, T.
M. Gosliner.

Etymology: The specific name glandulosa is chosen to
call attention to the yellow glandular structure occurring
distally on the extra-branchial appendages.

Distribution: Polycerella glandulosa has been found along
the Pacific coast of California from Morro Bay south to
San Diego. Within the Gulf of California it has been found
from the La Paz region north to Bahia de los Angeles.

Natural history: Polycerella glandulosa has generally been
collected in association with the ctenostomatous bryozoan
Zoobotryon sp. Specimens, together with egg masses, are
commonly found crawling on Zoobotryon colonies, on float-
ing docks, and in the shallow subtidal zone to a depth of
20 m. Specimens from Morro Bay were collected in as-
sociation with another bryozoan, Bugula sp.

External morphology: The living animals reach 8 mm
in length. The limaciform body is typically polycerid. It
is compressed laterally and is highly arched dorsomedially,
near the branchial region (Figures 1, 2A). The foot is
linear and tapers posteriorly into a bluntly pointed tail.
The anterior corners of the foot form a pair of triangular
points (Figure 2A). The head is rounded and bears round-
ed lobes laterally. The distinct, semicircular frontal veil
consists of 5 papillae. These papillae are simple, elongate,
and cylindrical, tapering to a point apically. There are 2
extra-branchial appendages, situated posterolaterally to
the branchial plume. These appendages are irregularly
ramified and are slightly swollen at the most distal ramus
(Figure 2B). This swelling is yellowish and glandular, and

Page 320

The Veliger, Vol. 30, No. 3

Figure 1

A and B. Living animal (8 mm in length) of Polycerella glandulosa sp. nov., collected from Mission Bay, San
Diego, California, November 1982. Photos by Jeff Hamann.

appears granular internally. The function of this organ is
unknown. The non-retractile rhinophores (Figure 2C) are
perfoliate with 3 or 4 lamellae. The clavus of the rhino-
phores is short, less than one-third of the entire rhinophore.
The shaft tapers slightly towards the clavus. The branchial
plume is semicircular and consists of 6 or 7 irregularly
bipinnate gills. The posterior 2 gills are smaller than the
anterior ones. The notum is ornamented with numerous
cylindrical papillae. The anus is situated within the bran-
chial plume. The genital apertures are located on the right
side of the body at approximately the level of the ante-
riormost portion of the branchial plume.

The ground color is translucent white to cream. The
notum bears a series of irregular subepidermal brown
streaks and blotches. The notum is covered with yellow-
white and dark brown specks. The living animals appear
dirty white in color and are exceedingly cryptic when on
colonies of Zoobotryon.

Digestive system: The buccal mass is well developed and
muscular. A pair of short, cylindrical salivary glands is
present at the juncture of the narrow esophagus with the
posterior portion of the buccal mass. The jaws (Figure
3A) are ovoid and brown in color. Their surface is or-

D. W. Behrens & T. M. Gosliner, 1988

Page 321

Figure 2

Polycerella glandulosa. A. Living animal drawn from color transparency, scale = 1.0 mm. B. Extra-branchial

process, scale = 0.25 mm. C. Rhinophore, scale = 0.5 mm.

namented with flattened polygonal rodlets (Figure 3B).
The radula is minute and details of its morphology are
discernible only by means of scanning electron microscopy.
The radular formula is 28-40 x 3-1-2-:0-1-2-3 in three
specimens examined. The shape and configuration of the
radular teeth varies from one end of the radula to the
other. The formative portion of the radula is widest and
tapers significantly towards the older portion. In the oldest
portion of the radula the inner two laterals are fused to
form a single elongate tooth with four denticles (Figure
4A). After approximately the 15th radular row, these two
laterals become entirely separate. More posteriorly, the
inner lateral teeth (Figure 4B) are roughly triangular in
shape, with simple apical and basal hook-shaped denticles.

The second lateral is largest with an acutely pointed, tri-
angular denticle near the apex. A thickened medial portion
runs basally to the triangular basal denticle. In the oldest
portion of the radula the third laterals are simply hook-
shaped teeth. More posteriorly, they are roughly rectan-
gular, devoid of denticles, with a thickened medial portion
(Figures 4C, D). In the older portion of the radula the
outer two teeth are elongate and sickle-shaped. More pos-
teriorly, the fourth tooth has a thickened base, while the
fifth tooth remains narrow and elongate.

Reproductive system (Figure 3C): The preampullary
duct is narrow and expands into a short, saccate ampulla.
More proximally the ampulla narrows into a postampul-

Page 322 The Veliger, Vol. 30, No. 3

AD p
Figure 3

Polycerella glandulosa. A. Jaw, x 200. B. Jaw rodlets, x 400. C. Reproductive system, scale = 1.0 mm: al, albumen

gland; am, ampulla; bc, bursa copulatrix; me, membrane gland; mu, mucous gland; n, nidamental opening; p, penis;
pr, prostate; rs, receptaculum seminis; v, vagina; vd, vas deferens.

Figure 4

Polycerella glandulosa. Scanning electron micrographs of radula. A. Oldest portion of radula. B. Middle of radula.
C and D. Newest portion of radula.

D. W. Behrens & T. M. Gosliner, 1988 Page 323

3162 15K¥Y kéae 38um “931604 13K¥ al, ade 34um

831603 15KY¥Y é6aa Siem 831605 15KY 3700

Page 324

lary duct that divides into the oviduct and vas deferens.
The oviduct enters the female gland mass in the vicinity
of the albumen gland. The uterine duct also emerges from
the female gland mass close to the oviduct. It continues as
a narrow duct to the base of the pyriform receptaculum
seminis, where it joins with the receptaculum duct. The
receptaculum duct joins the vaginal duct prior to their
common entrance into the thin-walled, spherical bursa
copulatrix. The narrow vagina is elongate and expands
immediately prior to its exit adjacent to the penis. The
albumen gland is the smallest portion of the female gland
mass. The membrane gland is slightly larger, consisting
of numerous whitish folds. The membrane gland is smooth,
with several distinct lobes. The female glands terminate
at the nidamental gonopore ventral to the vaginal and
penial apertures. The narrow vas deferens expands into
the large prostate gland a short distance from its division
from the ampulla. At its proximal end the prostate abruptly
narrows again into an ejaculatory segment. Its proximal
end contains several rows of minute, curved chitinous hooks.
No distinct penial papilla is present.

DISCUSSION

The genus Polycerella Verrill, 1881, includes species with
a narrow radula, consisting of more rows of teeth than
Polycera Cuvier, 1817, and smooth, rather than perfoliate,
rhinophores. In Polycerella, the jaws are less well developed
than in Polycera. Four species of Polycerella have been
described from the Atlantic coasts of North and South
America and the Mediterranean. FRANZ & CLARK (1972)
considered Polycerella davenporti Balch, 1899, to be a junior
synonym of P. emertoni Verrill, 1881. Ev. Marcus (1976)
stated that P. conyna Er. Marcus, 1957, and P. recondita
Schmekel, 1965, are also junior synonyms of P. emertoni.
This synonymy was also supported by SCHMEKEL &
PORTMANN (1982). Thus, there appears to be only one
species of Polycerella inhabiting the Atlantic and Medi-
terranean.

The present species differs significantly from Polycerella
emertoni in several aspects of its external anatomy. The

The Veliger, Vol. 30, No. 3

rhinophores are perfoliate, with 3 or 4 lamellae, rather
than smooth. The extra-branchial processes are ramified
rather than simple. There are only 3 gills in P. emertoni
and 6 or 7 in P. glandulosa. The papillae are longer and
more numerous in P. glandulosa than in P. emerton1.

There are also some significant internal differences sep-
arating the species. The radular teeth of Polycerella glan-
dulosa are thicker and more strongly developed than those
of P. emertoni. In P. emertoni the third lateral teeth are
elongate hooks, while in P. glandulosa they are short and
thick. There is only a single row of inner lateral teeth in
P. emertom, while there are two rows present in most of
the radula of P. glandulosa.

In view of the addition of P. glandulosa to Polycerella,
the genus must be expanded to include species with smooth
and perfoliate rhinophores. Polycera differs from Polycer-
ella in having numerous (12-17) densely packed rhi-
nophoral lamellae, a narrow radula with quadrate, rather
than elongate, outer lateral teeth, and strongly developed
jaws.

ACKNOWLEDGMENTS

We thank Jeff Hamann for first bringing this species to
our attention, based on specimens he collected from Mis-
sion Bay, California, in 1982. We also thank him for
permission to use his photograph of the living animal.
Mary Ann Tenorio and Marc Charnow of the California
Academy of Sciences kindly prepared the final scanning
electron micrographic prints and photos of the living an-
imal.

LITERATURE CITED

FRANZ, D. & K. CLARK. 1972. A discussion of the systematics,
reproductive biology, and zoogeography of Polycerella emer-
toni and related species (Gastropoda: Nudibranchia). Veliger
14(3):265-270.

Marcus, Ev. 1976. Marine euthyneuran gastropods from Bra-
zil (3). Stud. Neotrop. Fauna Environ. 11:5-23.

SCHMEKEL, L. & A. PORTMANN. 1982. Opisthobranchia des
Mittelmeers. Springer-Verlag: Berlin.

THE VELIGER

© CMS, Inc., 1988
The Veliger 30(3):325-328 (January 4, 1988) =e ee

Anatomical Information on Thorunna (=Babaina)
(Nudibranchia: Chromodorididae) from ‘Toyama Bay and
Vicinity, Japan
by

KIKUTARO BABA

Shigigaoka 35, Minami-11-jyo, Sango-cho, Ikoma-gun, Nara-ken, Japan 636

Abstract. Glossodoris florens Baba, 1949, was referred to the new genus Babaina by Odhner in Franc,
1968, but it was transferred to Thorunna Bergh, 1878, by Rudman, 1984. This species, the type of
Babaina, was studied again. It agrees with Thorunna proper in the anatomy of the genital system, but

it differs somewhat from Thorunna proper in details of the tooth morphology and shape of the oral
tube.

INTRODUCTION

Collections made from different stations of Japan during
recent years provided a number of both recorded and un-
recorded species of the Chromodorididae. This paper de-
scribes the taxonomy and anatomy of a species that has
not been extensively characterized before.

Thorunna florens (Baba, 1949); Hanairo-umiushi

(Figures 1-3)

Synonymy

Glossodoris florens BABA, 1949:53, 143-144, pl. 19, fig. 67,
text-fig. 60—Hayama, Sagami Bay; ABE, 1964:49, pl.
22, fig. 79 —Tsuruga Bay, etc.

Babaina florens: TAKAOKA BIOL. CLUB, 1978:6, photo (col-
or)—Abugashima, Toyama Bay.

Thorunna florens (Babaina florens): BABA, 1985:225, figs. 2F,
4F, 5F, 10—Echizen-cho, Echizen Coast; Ogi, Toyama
Bay; Togi-Kazanashi, Noto Pen.

See also:

Thorunna BERGH, 1878:575 (type: Thorunna furtiva Bergh,
1878— Philippines); RUDMAN, 1984:216, 225-226, 264.

Thorunna furtiva: RUDMAN, 1984:216-220, figs. 76, 77, 80—
Heron Is., etc., Australia.

Figure 1

Thorunna florens. A and B, from material no. 1. A. Entire animal

in actively crawling position, from above, total length 17 mm;

part of the dorsal tubercles and a branchial plume are shown B
enlarged. B. Same animal from below. r, reddish purple; w,

opaque white; y, yellow.

Page 326

The Veliger, Vol. 30, No. 3

Figure 2

Thorunna florens. A-D, from material no. 2; E, from material no. 1. A. Digestive system from above. B. Blood
gland (not to scale). C. Pharynx in frontal view (not to scale). D. Labial disc (not to scale). E. A transverse row
of radula. ca, caecum; in, intestine; L, liver; m?, main cusp; oe, oesophagus; st, stomach; tu, oral tube.

Babaina ODHNER in Franc, 1968:867 (type: Glossodoris flo-
rens Baba, 1949—Sagami Bay, Japan).

Main material: All the specimens were collected by the
Takaoka Biological Club. No. 1. Echizen-cho, Echizen
Coast, Japan, 11 Aug. 1966, 1 specimen, total length 17
mm (external figures and radula). No. 2. Ogi, Toyama
Bay, Japan, 5 Aug. 1962, 11 specimens, length 8-10 mm
preserved (digestive system, labial disc, and genital sys-
tem). Additional specimens were collected from many sta-
tions of the central Japan Sea coast between Sado Island
and Tsuruga Bay, since the year 1951.

Description: A small species. The upper surface of the
mantle is covered with minute conical tubercles. No mantle
glands are present. The simply pinnate gills, about 9 in
number, are set in a circle which is open behind.

An example of the color pattern of the body is shown
in Figure 1A. The ground color of the back is slightly
yellowish white, but a fleshy tint of the viscera shines
through the integument of the mid-dorsum. The chrome-
yellow stripe or band running down each side of the back
from behind the rhinophore to the rear of the branchial
circle is accompanied with an opaque white line on the
inside. This chrome-yellow band is usually entire, but is
sometimes discontinuous. A short chrome-yellow arc oc-
curs just in front of the rhinophores. The anterior edge of

the mantle is marked with a double band of chrome yellow
and opaque white. On the inside of the mantle margin
there is a row of reddish purple spots. Each rhinophore
is yellow on the club and whitish on the stalk. The gills
are whitish. Each plume is tinged with yellow on the
rachis. The tail end has a submarginal reddish purple
band. The underside of the body (Figure 1B) is colorless.

In Thorunna the pharynx is greatly reduced in size in
contrast to the large, elongate oral tube. In 7. florens the
oral tube (Figure 2A) is short, swollen, and bulbous. The
cuticular labial disc appears to be naked. The radula is
extremely small with the formula of 33 x 20-25.0.20-25.
In Thorunna proper the first lateral tooth is somewhat
stronger than the next lateral teeth. In 7. florens, however,
all the lateral teeth are similarly elongated (Figure 2E),
narrow, and spatular in shape. In constitution the first
lateral tooth has two denticles on the inside of the main
cusp and the next lateral teeth have each a single denticle
on the inside of the main cusp. In 7. florens, both these
cusps and denticles tend to become finer and rather un-
usually tapering to the tips. A stomach caecum is present
in 7. florens. The blood gland lies on the oesophagus just
behind the nerve center.

The genital system of Thorunna florens is fundamentally
as in Thorunna proper (Figure 3). That is, the spermato-
cyst is sausage-shaped, and the spermatheca is larger and

K. Baba, 1988

D

Page 327

Figure 3

Thorunna florens. A-D, from material no. 2. A. Main part of the genital system from above. B. Oviducal part
analyzed. C. Vestibular gland in surface view. D. Vaginal part analyzed. am, ampulla; c, spermatocyst; fm, female
gland mass; hd, hermaphrodite duct; is, insemination duct; mo, male orifice; ov, oviduct and oviducal orifice; p,
penis; pr, prostate; t, spermatheca; v, vagina; vd, vas deferens; z, vestibular gland.

spherical. There is a well-developed vestibular gland lead-
ing to the oviducal vestibulum. The vagina is slender, but
it is not winding. The penis is unarmed.

Remarks: Babaina as represented by Thorunna florens may
be synonymized with Thorunna following RUDMAN (1984):
T. florens agrees with Thorunna proper (e.g., T. furtiva) in
the marked development of a vestibular gland. However,
it is noted that 7. florens differs more or less from Thorunna
proper in the shape of the first lateral tooth, which is not
differentiated in size from the rest of the lateral teeth of
the radula. The cusps and denticles on the lateral teeth
are apt to be tapering to the tips. The bulbous oral tube

of T. florens is also different from the elongate oral tube
of Thorunna proper. The rodlets of the labial disc in Tho-
runna proper that were mentioned by Rudman (1984)
were not seen in my mounted specimen. Thus, 7. florens
is a somewhat rare example of a species that may be
included in the genus 7horunna in an expanded sense.

ACKNOWLEDGMENTS
My thanks are due to the members of the Takaoka Bio-
logical Club, Toyama-ken, Japan, for affording me spec-
imens for field and laboratory study. The manuscript of
this paper was critically read and improved by two anon-
ymous reviewers.

Page 328

LITERATURE CITED

ABE, T. 1964. Opisthobranchia of Toyama Bay and adjacent
waters. Hokuryu-Kan: Tokyo. 99 pp., 36 pls.

BaBA, K. 1949. Opisthobranchia of Sagami Bay, collected by
his Majesty the Emperor of Japan. Iwanami Shoten: Tokyo.
194 pp., 50 pls.

BaBA, K. 1985. An illustrated key to the Chromodoridinae
genera of Japan (Mollusca: Nudibranchia: Dorididae). Shells
and Sea Life 17(10):225-228.

BERGH, R. 1878. Malacologische Untersuchungen. Jn: C. Sem-

The Veliger, Vol. 30, No. 3

per (ed.), Reisen im Archipel der Philippinen. Wiss. Res.
2(13):547-601, pls. 62-65.
ODHNER, N. 1968. Opisthobranches. Jn: P. Grassé (ed.), Franc,
Gastéropodes. Traité Zool. 5(3):834-893, pls. 10-11.
RuDMAN, W. B. 1984. The Chromodorididae (Opisthobran-
chia: Mollusca) of the Indo-West Pacific: a review of the
genera. Zool. Jour. Linn. Soc. 81:115-273.

TAKAOKA BIOLOGICAL CLUB. 1978. Photographic illustration
of the Opisthobranchia on the central Japan Sea coast. 53
pp., 1 map (in Japanese).

The Veliger 30(3):329-330 (January 4, 1988)

PE VELIGER
© CMS, Inc., 1988

Notes, Information & News

California Malacozoological Society

California Malacozoological Society, Inc., is a non-profit
educational corporation (Articles of Incorporation No.
463389 were filed 6 January 1964 in the office of the
Secretary of State). The Society publishes a scientific quar-
terly, The Veliger. Donations to the Society are used to
pay a part of the production costs and thus to keep the
subscription rate at a minimum. Donors may designate
the Fund to which their contribution is to be credited:
Operating Fund (available for current production); Sav-
ings Fund (available only for specified purposes, such as
publication of especially long and significant papers); or
Endowment Fund (the income from which is available.
The principal is irrevocably dedicated to scientific and
educational purposes). Unassigned donations will be used
according to greatest need.

Contributions to the C.M.S., Inc., are deductible by
donors as provided in section 170 of the Internal Revenue
Code (for Federal income tax purposes). Bequests, lega-
cies, gifts, and devises are deductible for Federal estate and
gift tax purposes under sections 2055, 2106, and 2522 of
the Code. Upon request, the Treasurer of the C.M.S., Inc.,
will issue suitable receipts which may be used by donors
to substantiate their tax deductions.

Subscription Rates and Membership Dues

At its regular Annual Business Meeting on 8 October
1987, the Executive Board of the California Malacozoo-
logical Society, Inc., set the subscription rates and mem-
bership dues for Volume 31 of The Veliger. For affiliate
members of the Society, the subscription rate for Volume
31 will be US$28.00; this now includes postage to domestic
addresses. For libraries and nonmembers the subscription
rate will be US$56.00, also now with postage to domestic
addresses included. An additional US$4.00 is required for
all subscriptions sent to foreign addresses, including Can-
ada and Mexico.

Affiliate membership in the California Malacozoologi-
cal Society is open to persons (no institutional member-
ships) interested in any aspect of malacology. There is a
one-time membership fee of US$2.00, after payment of
which, membership is maintained in good standing by the
timely renewal of the subscription.

Send all business correspondence, including subscription
orders, membership applications, payments for them, and
changes of address to C.M.S., Inc., P.O. Box 9977, Berke-
ley, CA 94709.

Page Charges

Although we would like to publish papers without charge,
high costs of publication require that we ask authors to
defray a portion of the cost of publishing their papers in
The Veliger. We wish, however, to avoid possible financial
handicap to younger contributors, or others without fi-
nancial means, and to have charges fall most heavily on
those who can best afford them. Therefore, the following
voluntary charges have been adopted by the Executive
Board of the California Malacozoological Society: $30 per
printed page for authors with grant or institutional support
and $10 per page for authors who must pay from personal
funds (2.5 manuscript pages produce about 1 printed page).
In addition to page charges, authors of papers containing
an extraordinary number of tables and figures should ex-
pect to be billed for these excess tables and figures at cost.
It should be noted that even at the highest rate of $30 per
page the Society is subsidizing well over half of the pub-
lication cost of a paper. However, authors for whom the
regular page charges would present a financial handicap
should so state in a letter accompanying the original manu-
script. The letter will be considered an application to the
Society for a grant to cover necessary publication costs.

We emphasize that these are voluntary page charges and
that they are unrelated to acceptance or rejection of manu-
scripts for The Veliger. Acceptance is entirely on the basis
of merit of the manuscript, and charges are to be paid after
publication of the manuscript, if at all. Because these con-
tributions are voluntary, they may be considered by authors
as tax deductible donations to the Society. Such contri-
butions are necessary, however, for the continued good
financial health of the Society, and thus the continued
publication of The Veliger.

Reprints

While it was hoped at the “birth” of The Veliger that a
modest number of reprints could be supplied to authors
free of charge, this has not yet become possible. Reprints
are supplied to authors at cost, and requests for reprints
should be addressed directly to the authors concerned. The
Society does not maintain stocks of reprints and also cannot
undertake to forward requests for reprints to the author(s)
concerned.

Patronage Groups

Since the inception of The Veliger in 1958, many generous
people, organizations, and institutions have given our jour-
nal substantial support in the form of monetary donations,

Page 330

either to The Veliger Endowment Fund, The Veliger Op-
erating Fund, or to be used at our discretion. This help
has been instrumental in maintaining the high quality of
the journal, especially in view of the rapidly rising costs
of production.

At a recent Executive Board Meeting, we felt we should
find a way to give much-deserved recognition to those past
and future donors who so evidently have our best interests
at heart. At the same time, we wish to broaden the basis
of financial support for The Veliger, and thus to serve our
purpose of fostering malacological research and publica-
tion. Accordingly, it was decided to publicly honor our
friends and donors. Henceforth, donors of $1000.00 or
more will automatically become known as Patrons of The
Veliger, donors of $500.00 or more will be known as Spon-
sors of The Veliger, and those giving $100.00 or more will
become Benefactors of The Veliger. Lesser donations are
also sincerely encouraged, and those donors will be known
as Friends of The Veliger. To recognize continuing support
from our benefactors, membership in a patronage category
is cumulative, and donors will be listed at the highest
applicable category. As a partial expression of our grati-
tude, the names only of donors in these different categories
will be listed in a regular issue of the journal. Of course,
we will honor the wishes of any donor who would like to
remain anonymous. The Treasurer of the California Mal-
acozoological Society will provide each donor of $10.00 or
more with a receipt that may be used for tax purposes.

We thank all past and future donors for their truly
helpful support and interest in the Society and The Veliger.
Through that support, donors participate directly and im-
portantly in producing a journal of high quality, one of
which we all can be proud.

Notes to Prospective Authors

The increasing use of computers to prepare manuscript
copy prompts the following notes. We request that the
right margin of submitted papers be prepared “ragged,”
that is, not justified. Although right-justified margins on
printed copy sometimes look “neater,” the irregular spac-
ing that results between words makes the reviewer’s, ed-
itor’s, and printer’s tasks more difficult and subject to error.
Similarly, the automatic hyphenation capability of many
machines makes for additional editorial work and potential
confusion; it is best not to hyphenate words at the end of
a line. Above all, manuscripts should be printed with a
printer that yields unambiguous, high-quality copy. With
some printers, especially some of the dot-matrix kinds,
copy is generally difficult to read and, specifically, the
letters ‘‘a, p, g, and q” are difficult to distinguish, especially
when underlined as for scientific names; again, errors may
result.

Other reminders are (1) that three copies of everything

The Veliger, Vol. 30, No. 3

(figures, tables, and text) should be submitted to speed the
review process, and (2) absolutely everything should be
double-spaced, including tables, references, and figure leg-
ends.

Because The Veliger is an international journal, we oc-
casionally receive inquiries as to whether papers in lan-
guages other than English are acceptable. Our policy is
that manuscripts must be in English. In addition, authors
whose first language is other than English should seek the
assistance of a colleague who is fluent in English before
submitting a manuscript.

International Commission on
Zoological Nomenclature

The following applications have been received by the Com-
mission and have been published in Vol. 44, Part 1, of the
Bulletin of Zoological Nomenclature (23 March 1987).
Comment or advice on these applications is welcomed for
publication in the Bulletin and should be sent to the Ex-
ecutive Secretary, ICZN, % British Museum (Natural
History), London SW7 5BD, U.K.

Case No. 2563. Conus floridanus Gabb, 1869 (Mollusca:
Gastropoda): proposed conservation of the specific name
by the suppression of an unused senior subjective syn-
onym, Conus anabathrum Cross, 1865.

Case No. 2548. Harpa articularis Lamarck, 1822 (Mol-
lusca: Gastropoda): proposed conservation of the specific
name, which is threatened by the unused senior syn-
onyms Harpa delicata and Harpa urniformis Perry, 1811.

Western Society of Malacologists
1988 Annual Meeting

The 21st Annual Meeting of the Western Society of Mal-
acologists will be held in Darwin Hall on the campus of
Sonoma State University, Rohnert Park, California, 17-
21 July 1988. Contributed papers are welcome on any
aspect of molluscan neontology and paleontology, includ-
ing research on terrestrial, freshwater, and marine mol-
lusks.

In keeping with its long standing tradition of emphasis
on eastern Pacific molluscan faunas, the WSM will con-
vene two special Symposia: “Biogeography and Evolution
of the Molluscan Fauna of the Galapagos Islands” (Chaired
by Matthew J. James) and “Marine Plant-Molluscan
Herbivore Interactions” (Chaired by Cynthia Trowbridge,
Marine Science Center, Newport, Oregon 97365).

For further information and registration materials, con-
tact Matthew J. James, Geology Department, Sonoma
State University, Rohnert Park, California 94928. Tele-
phone: (707) 664-2301.

The Veliger 30(3):331-332 ( January 4, 1988)

THE VELIGER
© CMS, Inc., 1988

BOOKS, PERIODICALS & PAMPHLETS

Nudibranchs of Southern Africa
A Guide to Opisthobranch Molluscs of
Southern Africa

by TERRENCE GOSLINER. 1987. Sea Challengers, Mon-
terey, and Jeff Hamann, El Cajon. 136 pp. Price: $34.95
(plus 6% tax for California residents) and shipping charge.

This is an excellent book. Dr. Gosliner has written a
superbly informative text and has beautifully photo-
graphed a marvelous fauna. Nudibranchs of Southern Africa
is a field guide to be read; whether intensely studied or
casually perused, it is a remarkable learning experience.

The book can be conveniently divided into three parts.
The Introduction is a terse, comprehensive account of opis-
thobranch evolutionary history, defense mechanisms, feed-
ing, and reproduction. A discussion of the habits and char-
acteristics of the higher taxonomic units, hints of where
and how to see living opisthobranchs, and an insightful
discussion of the biogeography of opisthobranchs from
southern Africa complete the Introduction. The biogeog-
raphy section is especially well written. A table showing
graphically the faunal affinities of the opisthobranch taxa
in this region conveys much information and deserves care-
ful study. It demonstrates a classic faunal replacement
along a geographic and environmental gradient. Dr. Gos-
liner’s explanations about the distributional patterns of
these organisms are carefully argued; throughout the book,
his decisions and opinions are supported with ample evi-
dence.

Part two consists of a species list (including all known
species from southern Africa, not just the species discussed
in this book), excellent line drawings (rendered by Bill
Liltved) of representative living animals and significant
anatomical features, and a dichotomous key to the 268
species of opisthobranchs treated in this book. Heed the
author’s caveat that this key is to be used for living animals.

The third part, comprising the majority of the book, is
the Species Accounts. Each animal, whether identified
to species or not, is described with a definitive text. The
text summarizes the taxonomy (with synonyms or signif-
icant morphological characteristics), natural history, and
the occurrence and distribution of the species. It is ex-
tremely readable. Field guide descriptions usually tend to
be tediously repetitive, but this book has a polished, vari-
able text that does justice to the foudroyant evolutionary
diversity of opisthobranch mollusks. When I finished read-
ing the species accounts, I kept turning the pages, hoping
to find more!

The final pages of the book include references, a species
index, map of southern Africa (titling the book after a
geographic rather than political entity is an appreciated
sensitivity), and a list of sizes of the animals photographed

(hopefully these will be placed on the same page as the
text or illustration of the animal in future editions).

The book is dedicated to Mrs. Eveline Marcus. She
should be quite pleased, because it is a most worthy present.

Hans Bertsch

A History of Shell Collecting

by S. PETER DANCE. 1986. E. J. Brill: Leiden, The Neth-
erlands. 265 pp. + 32 pls. Price: 94 guilders (about
US$42.75).

This book is a revision of Dance’s Shell Collecting: an
Illustrated History published in 1966. As that first edition
has been out of print for a number of years, a revision was
undertaken. According to the author’s Preface, “although
substantially identical to the first edition the text has been
considerably rearranged and enlarged.” Perhaps the great-
est change has been in the illustrations, many of which
are different from those in the first edition. The history
itself has not been carried forward, however, and the text
still does not extend far into the twentieth century.

What is still presented in this second edition is an en-
joyable, informative account of the collectors, dealers, and
students of “shells,” from Aristotle in the fourth century
B.C. through the seminal works of Buonanni, Lister, and
Rumphius in the seventeenth century to Linnaeus, La-
marck, Cuming, and beyond (but, unfortunately, not much
beyond World War I). The reader is given a look at the
shell cabinets, catalogs, and publications of the early shell
collectors, most of whom collected for the beauty (and
sometimes the status) of their specimens and some later
for the scientific benefits as well.

In addition to the main body of text, the book contains
four appendices and an extensive bibliography. The first
two appendices (‘‘Shell cabinets of the early eighteenth-
century arranged by location and vocation of owners” and
“Shell books in 1948”’) are primarily of historical interest,
although those who frequent bookstores in search of old
books on shells may find the latter appendix useful today.

The third appendix, titled ““Conchology or malacol-
ogy ?,” is an interesting, if peculiar, explanation as to why
Dance has used “conchology” exclusively to signify the
study of mollusks throughout his book, “carried there by
logical reasoning.” Dance attempts to synonymize the terms
conchology and malacology, and therefore to establish a
preference for conchology because it is the older term.
Although this argument would seem to be a logical exten-
sion of the principle of priority, so essential in zoological
nomenclature, it is not, because the two terms simply are
not commonly held as strict synonyms. As Dance acknowl-

Page 332

edges (p. 199), how things stand today is that “. . . we still
have the terms conchology and malacology in use at the
same time, the former implying the study of shells merely,
the latter implying the study of the molluscan animals,
and, incidentally, their shells.” As such, the terms are not
identical but rather provide useful, commonly understood
shades of meaning. Indeed if one of the terms should be
deleted from our lexicon, a notion I do not advocate, a
strong functional argument could be made for deleting
conchology, as that term seems to be the one with the more
ambiguous meaning.

The fourth appendix is a “Guide to collections: a list of

The Veliger, Vol. 30, No. 3

some shell collections of scientific importance and their
present locations.”” This is not only of historical interest,
but may be useful as well to present-day taxonomists in
need of locating type collections.

Notwithstanding some specific flaws, among them an
annoyingly large number of typographical errors, A history
of shell collecting is a worthwhile book to have. This mal-
acologist greatly enjoyed gaining a historical perspective
on the study of mollusks and will appreciate having the
volume on the shelf for reference.

D. W. Phillips

Information for Contributors

Manuscripts

Manuscripts must be typed on white paper, 842” by 11”, and double-spaced throughout
(including references, figure legends, footnotes, and tables). If computer generated copy
is to be submitted, margins should be ragged right (z.e., not justified). To facilitate the
review process, manuscripts, including figures, should be submitted in triplicate. The
first mention in the text of the scientific name of a species should be accompanied by the
taxonomic authority, including the year, if possible. Underline scientific names and other
words to be printed in italics. Metric and Celsius units are to be used.

The sequence of manuscript components should be as follows in most cases: title page,
abstract, introduction, materials and methods, results, discussion, acknowledgments, lit-
erature cited, figure legends, figures, footnotes, and tables. The title page should be on a
separate sheet and should include the title, author’s name, and address. The abstract
should describe in the briefest possible way (normally less than 200 words) the scope,
main results, and conclusions of the paper.

Literature cited

References in the text should be given by the name of the author(s) followed by the
date of publication: for one author (Smith, 1951), for two authors (Smith & Jones, 1952),
and for more than two (Smith et al., 1953).

The “literature cited” section must include all (but not additional) references quoted
in the text. References should be listed in alphabetical order and typed on sheets separate
from the text. Each citation must be complete and in the following form:

a) Periodicals
Cate, J. M. 1962. On the identifications of five Pacific Mitra. Veliger 4:132-134.

b) Books

Yonge, C. M. & T. E. Thompson. 1976. Living marine molluscs. Collins: London.
288 pp.

c) Composite works

Feder, H. M. 1980. Asteroidea: the sea stars. Pp. 117-135. In: R. H. Morris, D. P.
Abbott & E. C. Haderlie (eds.), Intertidal invertebrates of California. Stanford Univ.
Press: Stanford, Calif.

Tables
Tables must be numbered and each typed on a separate sheet. Each table should be
headed by a brief legend.

Figures and plates

Figures must be carefully prepared and should be submitted ready for publication.
Each should have a short legend, listed on a sheet following the literature cited.

Text figures should be in black ink and completely lettered. Keep in mind page format
and column size when designing figures.

Photographs for half-tone plates must be of good quality. They should be trimmed off
squarely, arranged into plates, and mounted on suitable drawing board. Where necessary,
a scale should be put on the actual figure. Preferably, photographs should be in the
desired final size.

It is the author’s responsibility that lettering is legible after final reduction (if any)
and that lettering size is appropriate to the figure. Charges will be made for necessary
alterations.

Processing of manuscripts

Upon receipt each manuscript is critically evaluated by at least two referees. Based on
these evaluations the editor decides on acceptance or rejection. Acceptable manuscripts
are returned to the author for consideration of comments and criticisms, and a finalized
manuscript is sent to press. The author will receive from the printer two sets of proofs,
which should be corrected carefully for printing errors. At this stage, stylistic changes
are no longer appropriate, and changes other than the correction of printing errors will
be charged to the author at cost. One set of corrected proofs should be returned to the
editor.

An order form for the purchase of reprints will accompany proofs. If reprints are
desired, they are to be ordered directly from the printer.

Send manuscripts, proofs, and correspondence regarding editorial matters to: Dr. David W.
Phillips, Editor, 2410 Oakenshield Road, Davis, CA 95616 USA.

CONTENTS — Continued

Effect of eyestalk ablation on oviposition in the snail Lymnaea acuminata.
S. Ks SINGH AND) ReVASVAGAR WATE 18 0), /.0 sii ale a geen eta ee eae ee

A review of the genus Agaronia (Olividae) in the Panamic province and the
description of two new species from Nicaragua.
AL LOPEZ MICHEL MONTOVASAN Ds (WLIO) ORE Zia een ee eres

A review of the generic divisions within the Phyllidiidae with the description of
a new species of Phyllidiopsis (Nudibranchia: Phyllidiidae) from the Pa-
cific coast of North America.

(MERRENGE ME GosuINnER AND DAVID) Wi) BEEIRIENS) is eae nye aoe ne nnn in re

A new species of Gastropteron (Gastropoda: Opisthobranchia) from Reunion
Island, Indian Ocean.
MERRENCE ME GOsLINERVAND GARY Ge VVTIECTANS ais ersten Gees iene ena

The first record of Polycerella Verrill, 1881, from the Pacific, with the description
of a new species.
Davip W. BEHRENS AND TERRENCE M. GOSLINER ....................

Anatomical information on Thorunna (=Babaina) (Nudibranchia: Chromodori-
didae) from ‘Toyama Bay and vicinity, Japan.
IKIKUTARG’ BABA (2). Vn) ee es ee a ie nL sha De et ee ee ee an a

NOPESHMINEPORMATION SaINIEWV)S sae req tele terae eae eee
BOOKSVEE RIO DICAIES Say TNE Eile Sees eee eee

Jil FFU

a) V43
THE Uv

ISSN 0042-3211

|

VELIGER

A Quarterly published by

CALIFORNIA MALACOZOOLOGICAL SOCIETY, ING
Berkeley, California

R. Stohler, Founding Editor

Volume 30 April 1, 1988 Number 4
— 7 CONTENTS
QL The possible role of gut bacteria in nutrition and growth of the sea hare Aplysia.
wid Timothy Z. VITALIS, MARGOT J. SPENCE, AND THOMAS H. CAREFOOT ... 333
MOLL Penetration of the radial hemal and perihemal systems of Linckia laevigata
(Asteroidea) by the proboscis of Thyca crystallina, an ectoparasitic gas-
tropod. |
De Ae EGhOEF Ds ilie SMOUSE,, JRO AND, Jo Eo PEMBROKE 2755. 0h. 505: 342
Gastric contents of Fissurella maxima (Mollusca: Archeogastropoda) at Los Vilos,
Chile.
CEcILIA Osorio, M. ELIANA RAMIREZ, AND JENNIE SALGADO ........... 347
Variable population structure and tenacity in the intertidal chiton Katharina
tunicata (Mollusca: Polyplacophora) in northern California.
PINT Osean OM SIRPIBBING aes Meese teva Literal reenact! bcp war eels re das, Dome Sint 2)5)1
Observations on the larval and post-metamorphic life of Concholepas concholepas
(Bruguiére, 1789) in laboratory culture.
NE OW ESE Ele DLS ATEN Om re carte ne ENE yee cid a ead a spi Pb ag tye lone Bh amines 358
Spawning and larval development of the trochid gastropod Calliostoma ligatum
(Gould, 1849).
ANUANINT Tah VSICOTISTOINTS: 15, Bick do, Oahu ee merle te eR ts Cer See oe eee eR nem ae eae 369
Individual movement patterns of the minute land snail Punctum pygmaeum
(Draparnaud) (Pulmonata: Endodontidae).
ZANE DER Se AURVAND EDRUNOSBAUR gine Git: Qty ite Guys ci aie cs i wore a choo ateie 372

CONTENTS — Continued

The Veliger (ISSN 0042-3211) is published quarterly on the first day of July, October,
January and April. Rates for Volume 30 are $25.00 for affiliate members (includ-
ing domestic mailing charges) and $50.00 for libraries and nonmembers (including
domestic mailing charges). An additional $3.50 is required for all subscriptions sent
to foreign addresses, including Canada and Mexico. Further membership and sub-
scription information appears on the inside cover. The Veliger is published by the
California Malacozoological Society, Inc., % Department of Zoology, University of
California, Berkeley, CA 94720. Second Class postage paid at Berkeley, CA and
additional mailing offices. POSTMASTER: Send address changes to C.M.S., Inc.,
P.O. Box 9977, Berkeley, CA 94709.

MOR a

THE VELIGER

Scope of the journal
The Veliger is open to original papers pertaining to any problem concerned with mol-
lusks.

This is meant to make facilities available for publication of original articles from a
wide field of endeavor. Papers dealing with anatomical, cytological, distributional, eco-
logical, histological, morphological, physiological, taxonomic, etc., aspects of marine,
freshwater, or terrestrial mollusks from any region will be considered. Short articles
containing descriptions of new species or lesser taxa will be given preferential treatment
in the speed of publication provided that arrangements have been made by the author
for depositing the holotype with a recognized public Museum. Museum numbers of the
type specimen must be included in the manuscript. Type localities must be defined as
accurately as possible, with geographical longitudes and latitudes added.

Very short papers, generally not exceeding 500 words, will be published in a column
entitled “NOTES, INFORMATION & NEWS”? in this column will also appear notices
of meetings, as well as news items that are deemed of interest to our subscribers in
general.

Editor-in-Chief
David W. Phillips, 2410 Oakenshield Road, Davis, CA 95616, USA

Editorial Board

Hans Bertsch, National University, Inglewood, California

James T. Carlton, University of Oregon

Eugene V. Coan, Research Associate, California Academy of Sciences, San Francisco
J. Wyatt Durham, University of California, Berkeley

Terrence M. Gosliner, California Academy of Sciences, San Francisco
Cadet Hand, University of California, Berkeley

Carole S. Hickman, University of California, Berkeley

David R. Lindberg, University of California, Berkeley

James H. McLean, Los Angeles County Museum of Natural History
Frank A. Pitelka, University of California, Berkeley

Peter U. Rodda, California Academy of Sciences, San Francisco

Clyde F. E. Roper, National Museum of Natural History, Washington
Barry Roth, Santa Barbara Museum of Natural History

Judith Terry Smith, Stanford University

Ralph I. Smith, University of California, Berkeley

Wayne P. Sousa, University of California, Berkeley

T. E. Thompson, University of Bristol, England

Membership and Subscription
Affiliate membership in the California Malacozoological Society is open to persons (no
institutional memberships) interested in any aspect of malacology. As an affiliate member,
a person may subscribe to The Veliger for US $25.00 (Volume 30), which now includes
mailing charges to domestic addresses. There is a one-time membership fee of US $2.00,
after payment of which, membership is maintained in good standing by the timely renewal
of the subscription; a reinstatement fee of US $3.00 will be required if membership
renewals do not reach the Society on or before April 1 preceding the start of the new
Volume. If a receipt is required, a self-addressed, stamped envelope (or in the case of
foreign members, the envelope and two International Postal Reply coupons) should be
included with the membership or subscription request.

The annual subscription rate to The Veliger for libraries and nonmembers is US $50.00
(Volume 30), which now zncludes mailing charges to domestic addresses.

An additional US $3.50 is required for all subscriptions sent to foreign addresses,
including Canada and Mexico.

Memberships and subscriptions are by Volume only (July 1 to April 1) and are payable
in advance to California Malacozoological Society, Inc. Single copies of an issue are US
$25.00 plus postage.

Send all business correspondence, including subscription orders, membership applications,
payments for them, changes of address, to: C.M.S., Inc., Post Office Box 9977, Berkeley,
CA 94709, USA.

Send manuscripts, proofs, books for review, and correspondence regarding editorial matters

to: Dr. David W. Phillips, Editor, 2410 Oakenshield Road, Davis, CA 95616, USA.

The Veliger 30(4):333-341 (April 1, 1988)

THE VELIGER
© CMS, Inc., 1988

The Possible Role of Gut Bacteria in Nutrition and
Growth of the Sea Hare Aplysia

by

TIMOTHY Z. VITALIS, MARGOT J. SPENCE,
AND THOMAS H. CAREFOOT

Department of Zoology, University of British Columbia, Vancouver, Canada V6T 2A9

Abstract.

The role of bacteria in nutrition and growth of the sea hare Aplysia was investigated by:

(1) comparing growth of Aplysia juliana Quoy & Gaimard on three algal diets in seawater media with
and without antibiotics, (2) assessing the number and types of bacteria in the guts of Aplysia dactylomela
Rang and A. juliana on different algal diets, (3) determining in vivo and in vitro effects of various
antibiotics on these bacteria, (4) measuring the degree to which bacteria isolated from the gut of A.
juliana break down various algal storage products and structural polysaccharides, and increase the pool
of free amino acids in a culture medium containing the green alga Ulva fasciata Delile, and (5) assessing
possible direct effects of antibiotics on the sea hare itself.

Aplysia juliana grew significantly less under antibiotic treatment (10 mg penicillin-G and 10 mg
streptomycin sulfate per L seawater) on each diet. The antibiotic treatment reduced the number of gut
bacteria in A. juliana by approximately one order of magnitude. Twelve colony types (assumed to
represent 12 bacterial types) were found in the gut of A. juliana and 23 different types in A. dactylomela.
Five bacterial types seemed to be residential in the two species and varied little with changes in diet.
Bacteria isolated from the gut of A. juliana were capable of breaking down carbohydrates in test media
and increasing the pool of free amino acids in a culture medium of the green alga Ulva fasciata. Neither
behavior nor rate of oxygen consumption in Aplysia was significantly affected by exposure to concen-
trations of antibiotics up to five times those employed in the growth studies, suggesting that the antibiotics
reduced the nutritional contribution of the bacteria by reducing their numbers in the gut, rather than
having a directly deleterious effect on the sea hares themselves. The results suggest that gut bacteria

may contribute significantly to nutrition and growth in Aplysia.

INTRODUCTION

The relationship between animals and their symbiotic gut
bacteria is well understood in vertebrates and in commer-
cially and medically important insects (BROOKS, 1964;
McBEE, 1971). In marine invertebrates, however, the re-
lationship is not as clear. Several recent studies on marine
invertebrate herbivores have pointed to a nutritional réle
for the gut bacteria (PRIM & LAWRENCE, 1975; FONG &
MANN, 1980; CAREFOOT, 1981a, b), although the extent
of nutritional contribution in some forms has been ques-
tioned (LAWRENCE, 1975; PRIM & LAWRENCE, 1975). FONG
& MANN (1980) showed clearly that amino acids produced
by gut bacteria in the sea urchin Strongylocentrotus droe-
bachiensis were absorbed from the gut and used in the
synthesis of the host’s own tissues. FISHER & CHILDRESS
(1986) also demonstrated that a large proportion (>45%)
of the carbon fixed by symbiotic chemautotrophic bacteria

inhabiting the gills of the gutless bivalve Solemya reidi is
translocated to, and used by, the host. In neither study was
the importance of such contribution to the host animal’s
overall nutrition investigated. Indirect evidence that the
sea hare Aplysia kurodai may employ bacterially produced
amino acids in its own nutrition was provided by CAREFOOT
(1981b). There, young animals maintained steady weight
on several chemically defined artificial diets with deficien-
cies in amino acids known to be essential for the rat, over
a 24-day experimental period. The most likely explanation
for this was that gut bacteria were providing the necessary
amino acid nutrients, assuming that sea hare requirements
for amino acids are the same as found for other animals.
Another study on juvenile A. dactylomela (CAREFOOT,
1981a) showed that animals eating a chemical diet deficient
in arginine (essential for the rat) and containing antibiotics
gradually lost weight over a 20-day period. ‘The weight
loss was reversed when the arginine-deficient diet was

Page 334
15
Ulva fasciata Without
Antibiotics
1O|F
= With
Antibiotics
5 . 7
a
By a
oo
al
O
Ulva reticulata
i Without
S&S) Antibiotics
rk 10
a=
iS)
i oe
= y), Antibiotics
: \
LW i~
= a?
ay

Enteromorpha sp.

= Without
10 Antibiotics
; With
|
BIL Vi, \Z Antibiotics
®

ZO
ee Fa

20 30
TIME (days)
Figure 1

Change in live weight of Aplysia juliana on diets of the green
algae Ulva fasciata, U. reticulata, and Enteromorpha sp., with and
without antibiotic treatment (10 mg streptomycin sulfate and 10
mg penicillin-G-L seawater!) at 25°C. Each point represents
the X + SE of six animals.

replaced by one complete in all nutrients. In vitro studies
by PRIM & LAWRENCE (1975), on the ability of bacteria
isolated from the guts of sea urchins to digest algae and
various storage products of algae, have further supported
the notion that symbiotic gut bacteria are generally in-
volved in the nutrition of marine invertebrate herbivores.
This contribution could be especially significant in in-

The Veliger, Vol. 30, No. 4

stances where less than optimally nutritious seaweeds or
other plants are eaten, where foods are particularly in-
digestible, or where for reasons of temporal or spatial
shortages a variety of seaweeds must be consumed.

The present study investigates the possible réle of gut
bacteria in the nutrition and growth of the sea hare Aplysia.
It involves five major approaches: (1) a comparison of
growth rates of animals treated and not treated with an-
tibiotics, (2) an assessment of the number and types of
bacteria in the guts of the sea hares, and whether these
change with change in diet, (3) an assessment of the effects
of various antibiotics on these bacteria, (4) a measure of
the degree to which algal storage products and structural
polysaccharides are broken down by bacteria isolated from
the guts of sea hares, and the extent to which bacteria can
increase the pool of free amino acids in an Ulva fasciata
culture medium, and (5) an assessment of the direct in-
hibitory effects, if any, that the antibiotics might have on
the sea hares themselves.

Effect of Antibiotic Treatment on Growth Rates

Individuals of Aplysia juliana were metamorphosed from
a single batch of eggs following procedures outlined in
SWITZER-DUNLAP & HADFIELD (1977). Forty-two ani-
mals were successfully metamorphosed. When they reached
a live weight of 0.15-0.30 g, 36 were divided into 6 groups
of 6 animals each, such that each group had approximately
the same mean live weight and variance (0.25 + 0.001 g).
Each group was kept in a plastic tub (10 x 10 x 14 cm)
and supplied with its own flow of seawater (33%0, 25°C).
The groups were randomly divided into three double sets
(control and experimental), each set receiving as food one
of the green seaweeds Enteromorpha sp., Ulva fasciata, or
U. reticulata Forsskal. After a 5-day holding period, the
experimental group in each set was treated with antibiotics
in an attempt to sterilize the animals’ digestive tracts. The
antibiotic treatment consisted of 10 mg streptomycin sul-
fate and 10 mg penicillin-G delivered per L of seawater
over the 28-day period of study. The antibiotics were ad-
ministered dropwise from a stock solution (containing 1 g
of mixed antibiotics per L seawater) into the seawater
flowing through the system. At the start of the antibiotic
treatment all animals were given rations just sufficient to
satisfy their appetites (based on data from previous growth
studies; CAREFOOT, 1970). This minimized “superfluous”
feeding (feeding in excess, which results in quicker passage
of food through the gut and less efficient digestion) and
thus ensured that the gut bacteria had maximal time to
act on the ingested algae. The animals were weighed every
few days over the 28-day experimental period.

Figure 1 shows change in live weight of Aplysia juliana
on three seaweed diets with and without antibiotics. In
each case, animals treated with antibiotics grew signifi-
cantly less than did untreated animals (P < 0.001, AN-
OVA). Animals grew fastest and showed greatest response
to the antibiotics on a diet of Ulva fasciata, the alga most

Page 335

T. Z. Vitalis et al., 1988

HGS wopuei

OAS 7 sureyo ou 19909 = Wyss jusiedsueny yjoouls SS9][1OJOO eNaalte) punos I-S0 +2
%09 wopurt 1/€
wOb pednois ou = UIPIM/yBug] ‘spor = WSs jusredsuesny yjoouws wieato aunua punol €-I €Z
aspa o14mM
pastes AJOA anbedo y}oouls ‘zaj}ua0 yurd oatua puno. Z ZZ
%08 wopuri WG
WOT sured ou = YIpIm/yisug] ‘spor — YSIS anbedo yjoouls aqyM ainua puno. $-] 1Z
auou —-» Juauedsueny yioours SS9[1O]OO ounua punos SOs 0Z
Wyss juoredsurs yioouls Se) 0) (0) repnsast JepnSa1it = BUIAIeA |
*wOOL wopue. ou 19909 + pastes AroA anbedo ysno1 Mo]oA IepnBo1I1 puno. Z g]
*OOT wopuri ou 19909 — 1YysIys anbedo ysnos MoO]JaA —s- paynjoauoo Jepnsoiit BurArea |
1/€
*wOOT wopurr sad = YIpIM/ySuy] ‘spor — ists — juoredsuey yoouls Ss) 80) (089) 241]U9 punor CG {-] 9]
1/Z yoours Jaqua9 yep
*OOT wopurs ou = YIPIM/ySuy] ‘spor = pastes anbedo Asso]3 UWIM ureaJ9 aimuo puno. €-Z Gy
*OOI wopues ou 19909 = YSIS anbedo yoours yoriq ounua puno. I +1
*wOOT wopur. ou spo. = Wyss juosredsuesy yyoous SS2J1OJOD ~— payNyOAUOD punos Z-I €]
YSIS anbedo y.OOUIS Auwieat9 aamua puno. [=Gi0ee GT.
#8 wopur. J9]u99 yep
ANY sated ou 19909 = Wyss juoredsursy yoouls ‘g8pa Aureaid = paynjoauoo Iepnso1I1 OL II
*OOT wopur. ou 19909 = poster juouedsueny yyoours SS9]IO]OO ounua punos I-S0 Ol
%OOI wopue. ou spor = Wyss AraA — yuaaedsuen yoous MOTJAA ated ~—s paynyoAUOD JepnSasst = Surdrea 4G
Asso]
*OOI wopue. ou 19909 = Wyss Ara anbedo yjoouls Moy]oA oinua puno. I-S0O 8
*OOI wopue ou 19909 — Wyss juoiedsurs ysnos Mo]Jad —s paynjoauoo repnSormt = BurArea
%0S wopurs 1/7
OS sureyo ou = YIPIM/yBug] ‘spor = 1YsIys anbedo yjooulrs asurio aanua puno. =] 9
= Wyss AtaA — uosedsuesn yoouls Auress ‘a5urso0 ainua IV[NBII1II Z G
wOr wopues
Ov SAAD
HOT saved ou 19909 = postes anbedo yyoouls MoT[IA ainue puno. I-S0. 36+
*wOOI wopue.l ou Japuag]s pue Buoy :spo. = WSs uoredsuen ysno1 Auwie9.19-MoT[aA oanua puno. 9-S S
HOE sjajdiy
OL sired ou 19909 = SITs anbedo yloours outyM oaua punor CG I-¢Q Z
CAS) wopues
HOT sated ou 19909 = JUsIs onbedo yjoours Aureaso ouua puno. €-Z I
jusWasueIly sul adeys ureys uoneAg[y 14st] ISI] payapyos uoneUsUIsIg UISIL IA adeys (wu) “ON
-WI0J weg poytusuen sapun Auojor BYAIS
-a10dg Japun Auojor
ASojoydsow Auojoo s1dossoss Vy ASojoydsour Auojoo o1doosos19e yy

‘(PL61) SNO#AI4) 29 NVNVHONG Wo
sonstiajoVIeyO aandiuosap prepuris (77-9 ‘p-] SON) Djawojdjovp “py pue (Q-] ‘SON) vuvynl viskidy Jo sins Jy WO] paze[OSI SaTUO]O [elIa}DKq JO uondtwosaqq

CLAD

Page 336

The Veliger, Vol. 30, No. 4

Table 2

Number and types of bacteria isolated from the guts of Aplysia. Values are based on the means of counts from 2 to 6
animals.

Total number of

Diet colony types Number

Aplysia juliana

Ulva spp. 12 6

Enteromorpha sp. 12 6
Aplysia dactylomela

Ulva fasciata 7 4

Spuridea sp. 17 5

Laurencia sp. 10 iT

starved (5 days) 11 4

artificial — —

preferred by field animals and one known to be a good
settlement-inducer in this species of sea hare (SwiT-
ZER-DUNLAP & HADFIELD, 1977). Overall, the antibiotic
treatment reduced growth of the animals by 40-53% on
the three diets. Neither diet nor the interaction of anti-
biotics and diet had a significant effect on growth rates
(P = 0.11 in each case, ANOVA). A pump malfunction in
the seawater system bathed the animals for one day with
supersaturated seawater (a leak caused air to be pumped
into the seawater under pressure), and this feeding inter-
ruption explains the conspicuous drop in weight shown by
all animals on day 26 of the experiment (see Figure 1).

Number and Types of Bacteria in the
Guts of Aplysia

At the end of the growth experiment the gut was dis-
sected from each Aplysia juliana and the total contents of
the crop and gizzard regions removed with a sterile Pasteur
pipette. The contents were diluted 1000-fold in autoclaved
seawater and an aliquot plated onto nutrient agar. The
culture medium consisted of 10 g bactopeptone (Difco), 15
g agar (Difco), and 1 L of membrane-filtered and auto-
claved seawater. To this was added 15 mL 50% w/v sep-
arately autoclaved glucose solution. Two culture media
were used, one with a pH of 6 to match that of the crop
of Aplysia, the other with a pH of 8 to match that of the
gizzard. The inoculated plates were incubated for 4 days
at 25°C, after which the colonies were counted and char-
acterized according to standard morphological features
(methods outlined in BUCHANAN & GIBBONS, 1974). The
bacteria were not identified as to species. Similar platings
were made from the guts of A. dactylomela feeding on
several algal diets, from some that had been starved for 5
days, and from ones eating a chemically defined artificial
diet.

Twenty-four colony types were identified in platings
from crop and gizzard contents of Aplysia juliana and A.
dactylomela (Table 1). In A. juliana, six of these isolates

Predominant colony types

Number of bacteria/mL

Identity (Nos. refer to Table 1) gut fluid
Nos. 1-6 43 x 105
Nos. 1-6 =
Nos 1, 2, 4,9 53 x 10°
Nos. 1, 7, 9, 10, 24 —
Nos. 1, 4, 7-9, 19, 24 —
Nos. 1, 4, 9, 24 —

ZoExXalO2

were abundant and appeared consistently (Nos. 1-6, Table
1; another six appeared in the A. juliana platings, but only
sporadically and in low numbers, and thus are not de-
scribed in Table 1). There was no obvious correlation
between the presence or absence of a bacterial type and
the diet or treatment (with or without antibiotics) in this
sea hare species. The number of bacteria was highly vari-
able, but averaged about 43 x 10°-mL gut fluid~' in
normal animals, and 4-10 x 10°-mL gut fluid~! in an-
tibiotic-treated animals.

In comparison, 23 bacterial types were identified in
platings from the buccal mass, crop, gizzard, and digestive
gland of Aplysia dactylomela. Of these, 4-7 types predom-
inated depending on diet, 4 of which were present in the
guts of animals starved for 5 days. There was no evident
correlation of bacteria types with seaweed diet in A. dac-
tylomela (Table 2). Animals starved for 5 days had 11
types spread through the various regions of the gut, as
many or more than in the guts of some normally feeding
animals. Of the 6 commonest types isolated from A. juliana,
5 appeared identical to types from A. dactylomela (Nos. 1-
4, 6; Table 1). All but one of the total of 24 different types
present in abundance in the two species of Aplysia had
Gram-negative staining characteristics. Finally, there was
no consistent pattern either in the types or numbers of
bacteria with the location in the gut in A. dactylomela.

Effect of Antibiotics on the Gut Bacteria

The effectiveness of antibiotics in reducing the numbers
of gut bacteria in Aplysia juliana was determined by treat-
ing six animals (11-14 g live wt) over a 6-day period with
seawater containing antibiotics (50:50 mix of streptomycin
sulfate and penicillin-G) in concentrations ranging from
0 to 1000 mg-L seawater~'. All animals were allowed to
feed ad libitum on Ulva fasciata and U. reticulata. The an-
imal in zero concentration of antibiotics was a control. At
the end of the 6-day period of treatment the gut contents
were removed and plated onto agar discs, as described

T. Z. Vitalis et al., 1988

Table 3

Resistance of selected bacterial types from the gut of Aply-

sta dactylomela (colony Nos. 10 and 24, Table 1) to various

antibiotics. The antibiotics were administered in the form

of Difco-discs containing standardized antibiotics dosages.

Response of the bacteria is indicated as S = susceptible,
I = intermediate susceptibility, and R = resistant.

reer Response of bacteria
Antibiotic (ug) No. 10 No. 24
Ampicillin 10 I I-S
Chloromycetin 10 S S
Erythromycin 5 I-S R
Kanamycin 10 I R
Neomycin 10 I-S R
Penicillin 3 R R
Polymycin B 10 I R
Streptomycin 5 R R
Tetracycline 10 R I-S

previously, and the total number of bacteria growing at
each dosage of antibiotics was counted.

Figure 2 shows the bacterial cell counts in relation to
antibiotic dosage. The antibiotics appeared to reduce
markedly the number of bacteria, even at comparatively
low dosages. The control Aplysia juliana had 43 x 10°
bacteria‘mL~! in its crop/gizzard, comparable to values
of 48 and 59 x 10° bacteria‘mL“'! counted in the digestive
contents of two specimens of A. dactylomela feeding on U.
Jasciata (see also Table 2). The A. juliana treated with 70
and 1000 mg antibiotics:L seawater! each had counts of
1 x 10° bacteria-‘mL gut fluid~'. Based on these obser-
vations and bacterial counts of animals used in the growth
experiments, the concentration of antibiotics used in the
growth experiment reduced the number of gut bacteria
approximately one order of magnitude.

Page 337

A number of antibiotics were tested in vitro for their
effectiveness against gut bacteria in Aplysia dactylomela.
Difco discs containing standard dosages of the antibiotics
ampicillin, chloromycetin, erythromycin, kanamycin, neo-
mycin, penicillin, polymycin B, streptomycin, and tetra-
cycline were tested against two of the most prevalent types
of bacteria found throughout the guts of sea hares (Nos.
10 and 24; see Table 1). The standard dosages in the discs
were 10 ug for all except erythromycin and streptomycin,
which were 5 wg, and penicillin which was 3 wg. The
response of Escherichia coli to the same antibiotics was used
as a standard of comparison for the responses of the Aplysia
gut bacteria. A standard test procedure was employed as
outlined in BUCHANAN & GIBBONS (1974).

The results of the Difco-disc series of experiments are
presented in Table 3. Ampicillin and chloromycetin were
the most effective antibiotics on the two bacterial types
tested. With the exception of some intermediate levels of
susceptibility of one or other of the bacterial isolates to
erythromycin, neomycin, and tetracycline, the bacteria were
generally resistant to all of the other antibiotics.

Utilization of Plant Constituents by
Aplysia Gut Bacteria

Utilization of various plant constituents by bacteria iso-
lated from the gut of Aplysia juliana was determined using
carbohydrate-vitamin-nitrogen (CVN) media as described
by PRIM & LAWRENCE (1975). Each CVN medium con-
tained a single carbohydrate source. Carbohydrates tested
included glucose, maltose, starch, carrageenan, and cel-
lulose. After a 4-day incubation at 25°C with each of the
six main bacterial types isolated from A. julzana, utilization
of a carbohydrate was judged to have occurred if the culture
medium turned cloudy, if sediment accrued at the bottom,
or if growth occurred at the surface (PRIM & LAWRENCE,
1975). CVN media without bacteria and inoculated CVN
media without a carbon source were used as controls. Each

Table 4

Utilization of carbohydrates by each of six types of bacteria isolated from the gut of Aplysia juliana. The bacteria were
incubated for 4 days at 25°C in carbohydrate-vitamin-nitrogen media at pH = 6 (as found in the crop of Aplysia) and
pH = 8 (gizzard).

Glucose Maltose
Bacterial isolate pH6 pH8 pH6 pH8
1 + + + +
2 - + - -
3 + + + 7
4 + 4 + +
5 + + + +
6 + + + +

Carbohydrate substrate

Starch Carrageenan Cellulose
pH6 pH8 pH6 pH8 pH6 pH8
- + + + - ~
+ 4 + + - -
+ + + + - -
4 4 + + - -

Control (no carbohydrate)
Control (no bacteria) = =

|

Page 338

Table 5

Concentration of free amino acids in 10-mL aliquots of
three Ulva fasciata media: one, incubated 4 days at 25°C
with a mixture of the six predominant bacterial types from
the gut of Aplysia juliana; the other, a sterile control me-
dium incubated 4 days at 25°C; the last, a fresh homogenate
of the seaweed. The final column gives the approximate
x-fold change in concentration of each amino acid re-
sulting from bacterial action. Dashes indicate no data
available. Amino acids in block type are those known to
be essential for the rat.

Concentration (uM) of free amino
acids in Ulva fasciata media

Control x -fold
(incubated Incubated change in
4 days Fresh 4 days amino acid
with no homoge- with gut concen-
bacteria) nate bacteria _ tration
ARGININE —_ trace 516 —
Alanine 17 62 319 +8
Aspartic acid 22 34 32 nil
Glutamic acid 23 14 214 +11
Glycine aD 59 661 +16
HISTIDINE trace 41 23 nil
ISOLEUCINE 10 12 — —
LEUCINE 16 16 —_ —
LYSINE 16 20 21 nil
METHIONINE vi — 134 +19
Ornithine 26 38 24 nil
PHENYLALANINE 10 7 107 +12
Proline — = 461 —
Serine 34 110 50 nil
Threonine 11 22 2 nil
TYROSINE 9 7 49 +6
VALINE = 173 114 nil

test of a carbohydrate was replicated three times at pH
values of 6 and 8, representing values recorded from the
crop and gizzard, respectively, of A. julzana.

Table 4 shows that all six bacterial isolates were able
to grow on the CVN media containing either glucose or
carrageenan at pH levels present in the crop and gizzard.
The maltose- and starch-containing media showed lack of
growth in some instances. Neither the cellulose-containing
medium nor the controls supported growth of any of the
bacteria.

In addition, the ability of the gut bacteria to digest
seaweed was tested; a change in the concentration of free
amino acids in the culture was used as a measure of bac-
terial activity. Two 50-mg samples of oven-dried (60°C)
Ulva fasciata were each mixed with separate 2.5-mL por-
tions of seawater to slurry consistency and autoclaved for
15 min. Following this, one sample (the control) was made
up to 10 mL with 3.75% sulfosalicylic acid in 0.2 N lithium
citrate buffer, sealed, and stored in the dark at 2°C. The
remaining sample was made up to 10 mL with autoclaved

The Veliger, Vol. 30, No. 4

seawater and inoculated with a mixture of the six pre-
dominant bacterial isolates from Aplysia juliana and in-
cubated for 4 days at 25°C. At the end of the 4-day period,
a third 50-mg sample of dried Ulva was homogenized in
0.2 N lithium citrate buffer and made up to 10 mL. All
three samples were then centrifuged at 13,000 RPM for
5 min at 0°C. Aliquots (100 wL) of the supernatant were
analyzed for the presence of free amino acids using a Beck-
man Model 118C amino acid analyzer.

Table 5 indicates that bacterial action markedly in-
creased the pool of free amino acids in a culture medium
containing only seawater and the alga Ulva fasciata. The
values for the test culture were compared with the averages
of values for control (no bacteria) and freshly prepared
homogenate. There was no consistent difference between
these last two media with respect to levels of free amino
acids, suggesting that the bacteriocidal sulfosalicylic acid
treatment had no, or only minor, chemically degrading
effect on any free amino acids originally present in the
homogenate. Several essential (for the rat) amino acids
showed marked increases in concentration following in-
cubation of the seaweed with the bacteria (methionine,
phenylalanine, tryosine, and possibly arginine), as did some
non-essential ones (alanine, glutamic acid, and glycine).
Several amino acids remained in much the same concen-
tration as at the start, while none showed any marked
decrease in concentration.

Other Effects of the Antibiotics

The question remains as to whether antibiotic treatment
had any effect on the sea hares beyond reducing their levels
of gut bacteria. The animals’ feeding behavior was not
inhibited by antibiotic treatment. None of the animals died
during the experiments and none showed evidence of poor
health. However, since this was a critical point in inter-
pretation of the results, a further experiment was per-
formed to show that metabolic rate was not markedly
affected by antibiotic treatment. Aplysia dactylomela was
used in this experiment instead of A. juliana, as none of
the latter was available. The two species are similar in
size and share common behavioral attributes (e.g., both
are nocturnal). Aplysia dactylomela readily eats the ulvoid
species favored as food by A. julzana and growth rates are
comparable in the two species. The experiment employed
an antibiotic concentration five times that in the A. juliana
growth study (a total of 100 mg antibiotics: L seawater“ '),
and tested the immediate effects of the antibiotics on oxygen
uptake. A flow-through respirometer system with a YSI
Model 58 Dissolved-Oxygen Meter was used to monitor
oxygen levels (see CAREFOOT, in press, for details of res-
pirometry methods). The antibiotics were administered
directly from a stock solution into the seawater line flowing
to the respirometer. An animal was allowed 30 min of
equilibration time in the respirometer before its rate of
oxygen uptake was measured. Then, to test for instanta-
neous effects of the antibiotics, a 1-h baseline level of
oxygen uptake was established before the supply of normal

T. Z. Vitalis et al., 1988

Page 339

seawater was switched to that containing antibiotics. Rates
of oxygen uptake were monitored for a further 2-h period
after the start of antibiotics administration. All measure-
ments were made between 1100 and 1400 h at a temper-
ature of 28.5°C during the animals’ normal daytime state
of quiescence.

Figure 3 shows that there were no apparent acute effects
of the antibiotics in oxygen consumption in Aplysia dac-
tylomela. Rates were maintained at a fairly constant level
of 3.75-3.85 mL O,-indiv-'-h~' (P = 1.00, ANOVA)
despite perfusion of antibiotics-containing seawater (five
times the concentration used in the growth experiment)
over the Aplysia. Because it took some time for the anti-
biotics-treated seawater to replace completely the normal
seawater in the respirometer flask, and because this varied
with each run (depending on volume of the flask and flow
rate), the data in Figure 3 were re-expressed to show the
rate of oxygen consumption in relation to the actual con-
centration of antibiotics. These data are presented in Fig-
ure 4 and again show no significant effect of the antibiotics
on the rate of oxygen uptake in Aplysia over short-term
exposure (P = 0.99, ANOVA). While a larger sample size
and further information on possible long-term effects of
the antibiotics on the metabolic rate in Aplysia would make
these results more convincing, the data do suggest that the
level of antibiotics employed in the growth study had no
directly deleterious effects on the sea hares.

DISCUSSION

Several points of interest emerge from these data. First,
antibiotic treatment significantly reduces the growth of
juvenile Aplysia juliana. Second, bacteria are abundant both
in the number of individuals and the types throughout the
gut of sea hares, including the buccal region, crop, gizzard,
and digestive gland. Finally, bacterial isolates from the gut
of A. juliana readily break down various plant constituents,
such as maltose, starch, and carrageenan, and increase the
concentration of free amino acids in a seaweed culture
medium.

These facts point to a possible nutritional contribution
by the gut bacteria to their hosts. However, an alternative
explanation is that the antibiotics directly inhibit growth
of juvenile sea hares. Of the two antibiotics used in the
growth study, penicillin is the least likely to produce growth-
inhibiting side-effects in metazoans. Its antibacterial ac-
tivity involves the disruption of formation of cross-linkages
in the structurally unique bacterial cell wall (FRANKLIN
& SNow, 1975) and its action appears to be specific against
bacteria (HAMMOND & LAMBERT, 1978). In comparison,
streptomycin affects bacteria more generally, inhibiting
protein synthesis on ribosomes by interfering with the cod-
ing sequence of amino acids in the elongating peptide
chains (HAMMOND & LAMBERT, 1978). Streptomycin is
known to inhibit specifically the incorporation into peptide
linkages of arginine, glutamic acid, histidine, phenylala-
nine, and threonine (FRANKLIN & SNow, 1975). The po-

60

£
(eo)

NUMBER OF BACTERIA
ml GUT FLUID“ (x 10°)

ine)

(e)

O 1 10 100

1000
TOTAL ANTIBIOTIC DOSE
(mg: 1")
Figure 2

Change in number of bacteria in the gut contents of Aplysza juliana
after a 6-day exposure to different concentrations of antibiotics
in the seawater bathing the animals, at 25°C. The antibiotic
solution was a 50:50 mixture of streptomycin sulfate and peni-
cillin-G in seawater. Solid dots, A. juliana; open dots, A. dacty-
lomela. The latter were normal (untreated with antibiotics) an-
imals feeding for the same length of time as A. juliana on the
same green alga foods, Ulva fasciata and U. reticulata, and are
included for comparison. Each point represents a single animal.

tency of a penicillin and streptomycin mixture results from
synergistic effects of the component antibiotics, which re-
duce bacterial cell counts more effectively than if either
antibiotic is used individually (BROWN et al., 1979). The
blocking of cross-linking in the peptidoglycan structure of
the bacterial cell wall by penicillin facilitates the movement
of streptomycin into the cell (BROWN et al., 1979). Of the
two antibiotics, then, streptomycin would appear to be
potentially most deleterious to the sea hares.

CHERNIN (1959) tested the effects of various antibiotics
on the freshwater snail Australorbis glabratus under axenic
conditions. He found that streptomycin stunted growth of
the snail at concentrations of 100 wg-mL~'. No inhibition
occurred at a concentration of 10 ug-mL~! (equivalent to
that used in the present study), and the author noted that
small additions of CaCl, to the culture medium negated
certain stress-induced behavioral effects caused by the an-
tibiotic, even at fairly high concentrations (100 ug:-mL™';
CHERNIN, 1959). Penicillin had no effect on growth of
Australorbis at concentrations up to 60 wg-mL~' (CHERNIN
& SCHORK, 1959; six times the concentration used in the
present study). Thus, if sea hares responded in a manner

Page 340

The Veliger, Vol. 30, No. 4

2.0

OXYGEN CONSUMPTION
(mi indiv~ h7")

EEE te EN EET

ANTIBIOTICS
ADDED HERE

120 180

TIME (min)

Figure 3

Effect of antibiotics on oxygen uptake in Aplysza dactylomela. After 60 min to establish a baseline level of oxygen
consumption, seawater containing 100 mg antibiotics-L~' (50 mg each of streptomycin sulfate and penicillin-G)
was introduced into the respirometer at normal rates of flow. Owing to a scarcity of animals only four experiments
were run. Animal weights ranged from 150 to 307 g live. All values for oxygen consumption (Vo,) were converted
to a standard animal weight of 200 g live using the equation Vo,(200 2) = 200/exper wt)°”?°: Vo, exper) (See CAREFOOT,
1987). Each point represents the X + SE. Temperature = 28.5°C.

similar to Australorbis, the decreased growth rate of Aplysia
juliana could not be attributed to an antibiotic effect. As
well, the relatively high concentration of calcium ions in
seawater could have ameliorated any potentially undesir-
able behavioral side-effects streptomycin might have had
on the sea hares.

Oxygen consumption measurements on Aplysia dacty-
lomela treated with five times the concentration of anti-
biotics employed in the A. juliana growth study showed no
significant deviations from baseline values. If the antibiotic
treatment had created stress or caused illness in the sea
hares it would presumably have been manifested as a change
in metabolic rate, reflected in either increased or decreased
levels of oxygen consumption. As noted earlier, the animals
appeared to be normal throughout the growth experiment
and, even when subjected to a 50-fold greater concentration
of antibiotics than that used in the growth experiment
(Figure 2), the sea hares showed no observable change in
activity or in the rate of feeding. While these observations
are circumstantial, they nonetheless support the idea that
the negative effects of the antibiotics on the growth of A.
juliana were indirect effects due to a reduction in the num-
bers of gut bacteria, and not directly deleterious effects on
the sea hares themselves.

Bacteria certainly seem to be involved in the breakdown
of plant materials in the guts of marine invertebrate her-
bivores. They have been shown capable of releasing glucose
from carbohydrate storage materials such as maltose and
starch, and from such structural materials as carrageenan
(but not cellulose) during in vitro studies using bacteria

from sea urchins (PRIM & LAWRENCE, 1975) and bacteria
from sea hares (present study, see Table 4). In addition,
bacterial isolates from the gut of Aplysia juliana have been
shown in the present study to increase the concentration
of free amino acids in an Ulva fasciata culture medium.
The absorption and utilization of such bacterially produced
amino acids and fixed carbon by host animals in the syn-
thesis of their own tissues have been demonstrated in the
sea urchin Strongylocentrotus droebachiensis (FONG &
MANN, 1980) and the gutless bivalve Solemya reidi (FISHER
& CHILDRESS, 1986). While no similar experiments have
been done with sea hares, it can be expected that any
bacterially mediated breakdown product of seaweeds,
whether glucose or amino acids, would be readily absorbed
and used by an animal in its own metabolism. Indeed,
there could even be a degree of exploitative competition
for food resources occurring within the gut between the
bacteria and host.

The sea hare has several possible sources of amino acids
due to bacterial activity: (1) from normal extracellular
digestion of algal protein by the bacteria, (2) from synthesis
by bacteria and the release to the gut lumen, (3) from
digestion of bacteria by other bacteria, (4) from autolysis
of bacteria, and (5) from digestion of bacteria by the sea
hare’s own digestive enzymes. The high steady-state con-
centration of gut bacteria (even in starved animals), com-
bined with their diversity, point to a potentially important
role played by them in the nutrition of their hosts. FONG
& MANN (1980) suggest, in this regard, that the ability
of sea urchins to use a wide variety of seaweeds as foods

MeeZ= Vitalisreiial 98s

=
fo)

OXYGEN CONSUMPTION (mI: indiv-?-h7’)
iN
(oe)

O 50 100

CONCENTRATION OF ANTIBIOTICS (mg-1!7')

Figure 4

Relationship of oxygen consumption to antibiotics concentration
in Aplysia dactylomela. Data from the experiment outlined in
Figure 3. Regression statistics for the equation Y = a + bX are
a = 3.74 and b = —0.093. The correlation coefficient r = —0.138
is not significantly different from zero (P > 0.50).

stems from the clandestine nutritional contributions made
by bacterial symbionts.

In summary, antibiotic treatment inhibited growth of
juvenile sea hares either through an unknown and unob-
served directly deleterious effect or through an indirect
effect of nutrient loss through reduction in the number of
gut bacteria. The post-metamorphic rate of growth is high
in sea hares, and thus demand for amino acids is high.
Removal of gut bacteria, a potential source of amino acids
and glucose beyond those available from the breakdown
of algal protein, would limit the rate of protein synthesis
and metabolism and thus limit growth. We showed an
approximately one order of magnitude reduction in the
number of gut bacteria in Aplysia after treatment with
antibiotics. This is considerably less than the five orders
of magnitude reduction shown by FONG & MANN (1980)
to occur in the sea urchin Strongylocentrotus droebachiensis
after 2 days of treatment with the same antibiotics (but
using a higher concentration: 90 mg-L seawater!) but,
nevertheless, represents a considerable reduction in bac-
terial numbers. We believe that gut bacteria do contribute
significantly to the nutrition of Aplysia, as they seem to do
for other marine invertebrate herbivores, and represent a
factor largely neglected in past studies of growth, nutrition,
and dietary preferences in marine invertebrate herbivores
in general.

ACKNOWLEDGMENTS

We thank Robert Kane, Director of the Kewalo Marine
Laboratory, University of Hawaii, and Wayne Hunte,

Page 341

Director of the Bellairs Research Institute of McGill Uni-
versity, for providing research space and facilities. We are
grateful to Marilyn Switzer-Dunlap for use of her research
facilities, for supplying us with newly metamorphosed
Aplysia juliana, and for teaching us the fine art of rearing
A. dactylomela. We also thank Francis of Speightstown for
special laboratory assistance during the Barbados part of
the study and Barbara Taylor for helpful comments on
the manuscript. The research was supported by Natural
Science and Engineering Research Council of Canada
Summer Research Fellowships to T. Vitalis and M. Spence,
and by an operating grant from NSERC to T. Carefoot.

LITERATURE CITED

Brooks, M. A. 1964. Symbiotes and the nutrition of medically
important insects. Bull. World Health Org. 31:555-559.

Brown, M. R. W., P. GILBERT & R. M. M. KLEMPERER. 1979.
Influence of the bacterial cell envelope on combined antibiotic
action. Pp. 69-86. In. J. D. Williams (ed.), Antibiotic in-
teractions. Academic Press: London. 183 pp.

BUCHANAN, R. E. & N. E. GIBBONS (eds.). 1974. Bergey’s
manual of determinative bacteriology. Williams and Wil-
kins Co: Baltimore. 1268 pp.

CarReEFooT, T. H. 1970. A comparison of absorption and uti-
lization of food energy in two species of tropical Aplysia.
Jour. Exp. Mar. Biol. Ecol. 5:47-62.

CarEFooT, T.H. 1981la. Nutrition of a coral rubble-inhabiting
herbivore, the sea hare Aplysia. Proc. Fourth Intl. Coral Reef
Symp., Manila, 1981, 2:665-669.

CAREFOOT, T. H. 1981b. Studies on the nutrition and feeding
preferences of Aplysia: weight changes on artificial diets de-
ficient in specific amino acids. Can. Jour. Zool. 59:445-454.

CaREFOOT, IT. H. In press. Diet and its effect on oxygen uptake
in the sea hare Aplysia. Jour. Exp. Mar. Biol. Ecol.

CHERNIN, E. 1959. Cultivation of the snail, Australorbis gla-
bratus, under axenic conditions. Ann. N.Y. Acad. Sci. 77:
237-245.

CHERNIN, E. & A. R. ScHORK. 1959. Growth in axenic culture
of the snail, Australorbis glabratus. Amer. Jour. Hyg. 69:146-
160.

FIsHER, C. R. & J. J. CHILDRESS. 1986. Translocation of fixed
carbon from symbiotic bacteria to host tissues in the gutless
bivalve Solemya reidi. Mar. Biol. 93:59-68.

Fonc, W. & K. H. Mann. 1980. Role of gut flora in the
transfer of amino acids through a marine food chain. Can.
Jour. Fish. Aquat. Sci. 37:88-96.

FRANKLIN, T. J. & G. A. SNow. 1975. Biochemistry of anti-
microbial action. Chapman and Hall: London. 224 pp.
HAMMOND, S. M. & P. A. LAMBERT. 1978. Antibiotics and
antimicrobial action. Edward Arnold: London. 63 pp.
LAWRENCE, J. M. 1975. On the relationships between marine
plants and sea urchins. Oceanogr. Mar. Biol. Ann. Rev. 13:

213-2806.

McBeg, R. H. 1971. Significance of intestinal microflora in
herbivory. Ann. Rev. Ecol. Syst 2:165-176.

Prim, P. & J. M. Lawrence. 1975. Utilization of marine
plants and their constituents by bacteria isolated from the
gut of echinoids (Echinodermata). Mar. Biol. 33:167-173.

SWITZER-DUNLAP, M. & M.G. HADFIELD. 1977. Observations
on development, larval growth and metamorphosis of four
species of Aplysiidae (Gastropoda: Opisthobranchia) in lab-
oratory culture. Jour. Exp. Mar. Biol. Ecol. 29:245-201.

The Veliger 30(4):342-346 (April 1, 1988)

THE VELIGER
© CMS, Inc., 1988

Penetration of the Radial Hemal and Perihemal Systems of

Linckia laevigata (Asteroidea) by the Proboscis of

Thyca crystallina, an Ectoparasitic Gastropod

by

D. A. EGLOFF, D. T. SMOUSE, Jr., AND J. E. PEMBROKE

Department of Biology, Oberlin College, Oberlin, Ohio 44074, U.S.A.

Abstract.

The proboscis of female 7hyca crystallina (Mollusca) penetrates the body wall of Linckia

laevigata (Echinodermata) and terminates in the middle of the ambulacral ridge where it opens within
the perihemal sinus near the radial hemal strand. The proboscis does not penetrate the perivisceral
coelom of its host, nor can it be withdrawn because the attachment disc of the adult snail is fused to
the epidermis of the host. Except for a partial alteration in size and texture of a few ambulacral ossicles,
and loss or reduction in size of the host’s ampullae at the site of infection, other host organs and tissues
are relatively unaffected by the penetration of the proboscis. Presumably 7. crystallina obtains nutrients

from the hemal-perihemal systems of its asteroid host.

INTRODUCTION

Because females of the ectoparasitic snail Thyca crystallina
(Gould, 1846) are fused to their hosts, Linckia laevigata
(Linnaeus), lack mouth parts, and have reduced digestive
and enlarged salivary glands, many authors have concluded
that they must be utilizing nutrients not requiring complex
digestion (SARASIN & SARASIN, 1887; KUKENTHAL, 1897;
KOEHLER & VANEY, 1912; ADAM, 1934; CHENG, 1964).
To this extent the snail-host relationship has been well
described. However, both early and more recent published
discussions (TAYLOR & LEWIS, 1970; YONGE & THOMPSON,
1976; ELDER, 1979) have not described the pathway of
the snail’s proboscis into the host. Most investigators have
heretofore asumed that 7. crystallina sucks internal fluids
or tissues from L. laevigata but have not identified the
probable source of nutrients for the snail.

In the Echinodermata, nutrient transport from sites of
intake or storage has been attributed to one or more of the
following coelomic derivatives: the perivisceral coelom, the
water vascular system, the hemal system, and the perihe-
mal system (HYMAN, 1955; ANDERSON, 1966; FERGUSON,
1969, 1982; Binyon, 1972). To the extent that any or all
of these systems are rich in nutrients, they could serve as
a potential source of nutrients for Thyca crystallina.

In the present study we traced the route of penetration
of an ectoparasitic snail’s proboscis into a sea star’s arm
to determine which of the host’s internal systems are con-

tacted. Our discovery that the snail’s proboscis terminates
within the perihemal system near the radial hemal strand
suggests that these systems serve as a source of nutrients
for Thyca crystallina.

MATERIALS anpD METHODS

Specimens of the sea star Linckia laevigata were examined
from collections made in May 1965, December 1970, and
August 1976 on the reef flats east of the ship channel at
Suva, Fiji. Thirty-two specimens of the 224 (14.3%) col-
lected in 1965 were infected by one or more individuals
of Thyca crystallina (a limpetlike prosobranch gastropod
in the family Capulidae). Specimens were examined alive
or were preserved in buffered 4% formaldehyde. Gross
dissections were prepared with the aid of razor blades or
a small, motor-driven, circular saw. Specimens for sections
were decalcified for 2-3 days in a modified Heidenhain’s
Susa fixative (10 mL glacial acetic acid, 50 mL 40% form-
aldehyde, and 20 g trichloroacetic acid in 200 mL 70%
ethyl alcohol), embedded in paraffin in a low vacuum,
sectioned at 10-16 um, and stained with hematoxylin and
Gomori’s trichome or in Cason’s rapid one-step Mallory-
Heidenhain.

RESULTS

We found that female specimens of Thyca crystallina are
attached to their hosts by a circular disc as described by

D. A. Egloff et al., 1988

ADAM (1934). We also found the males of this species
attached under the shell of the females. The proboscises
of the males that we examined lay freely in the space under
the female shell and did not penetrate the integument of
the sea star.

The attachment discs of the female 7hyca crystallina are
fused in the largest specimens to the host’s integument by
fibrous connective tissues. The female proboscis extends
from the center of this attachment disc through a hole up
to 1 mm in diameter into the tegument of the host. Gross
dissections revealed that the proboscis enters the sea star’s
arm between the marginal dermal ossicles, progresses
through the thick connective and muscular tissue of the
dermis, and terminates in the middle of the ambulacral
ridge (Figures 1, 2A). By angling towards the ambulacral
ridge, the proboscis bypasses the perivisceral coelom, pen-
etrates the thick body wall, and enters the ambulacral
ossicles so that one or more ampullae of the host’s water
vascular system are lost or displaced. The only superficial
evidence of the proboscis on the internal surface of the
ambulacral ridge is the absence or reduction in size of 1-
3 ampullae and a darkening of the ambulacral ridge in
the area directly overlying the infected area; inside the
ambulacral ridge this may involve the reduction in size of
2-4 ambulacral ossicles on the infected side. Discoloration
results from a replacement of the ambulacral ossicle(s)
lying above the proboscis by an abnormal area of hyper-
trophied muscular and connective tissue. These alterations
in the ambulacral ossicle may be seen by comparing Fig-
ures 2B and C.

In 3 of 18 dissected specimens we observed a small hole
in the depression on the aboral side of the ambulacral ridge
in the middle of the discolored, infected area. In another
specimen we found a small hole opening downward from
the proboscis area into the ambulacral groove. Because
these openings were not present in most specimens nor in
any of the 12 sectioned specimens we assume they do not
represent the normal condition.

The proboscis of female 7hyca crystallina terminates in
the area occupied by the hemal and perihemal systems.
When uninfected areas are viewed in cross-section, these
systems form a triangular area bounded on the lower side
by the V-shaped radial nerve and on the upper side al-
ternately by the lower transverse ambulacral muscle and,
in the spaces between the muscles, by the radial water
canal (Figure 2C). These relationships are identical in
infected arms of Linckia laevigata proximal and distal to
the infection site, z.e., there is no histological evidence that
the ectoparasite affects the radial systems of the host on
either side of the point of infection. However, in the area
penetrated by the proboscis, an extensive displacement of
all systems occurs. The radial water canal is pushed to
one side and the radial nerve is flattened and also pushed
to the far side of the ambulacral groove; hemal tissues are
often more abundant in the region near the end of the
proboscis (Figure 2B). Despite the enlargement of the
hemal tissue, we traced the perihemal sinus through the

Page 343

Figure 1

Schematic cross-sectional view of an arm of Linckia laevigata to
which an ectoparasitic 7hyca crystallina is attached. View is to-
wards the central disc of the sea star. The snail’s proboscis by-
passes the perivisceral coelom, displaces 1-3 ampullae, penetrates
the radial perihemal sinus, but does not interrupt the water
vascular or nervous systems. 7hyca crystallina: 1, shell; 2, colu-
mellar muscle; 3, capsule gland; 4, digestive gland; 5, nephridium;
6, salivary gland; 7, attachment disc, left anterior edge; 8, pro-
boscis; 9, esophagus. Linckia laevigata: 10, hemal tissue; 11, peri-
hemal sinus; 12, radial water canal; 13, ambulacral ossicle; 14,
epidermis; 15, dermal ossicle; 16, ampulla; 17, dermis; 18, tube
foot; 19, radial nerve; 20, perivisceral coelom; 21, papula.

infected area beween unaltered distal and proximal regions
in 11 serially sectioned specimens. In a 12th specimen the
hemal tissue filled the space in front of the proboscis,
thereby locally obliterating the perihemal sinuses.

The proboscis of Thyca crystallina consists of a sheath
through which extends two salivary gland ducts and a thin-
walled esophagus that terminates in a thick-walled pha-
ryngeal mass (Figure 2D). In preserved specimens the wall
of the proboscis is contracted and therefore highly folded
in longitudinal sections. Except for a distinct outer epi-
thelium, the proboscis is filled with connective tissue, blood,
and blood cells. At its distal end the proboscis is folded on
its outer surface, forming a groove that encloses tissues of
the host (Figure 2E). This groove is continuous with the
internal proboscis space through which runs the pharyn-
geal mass and esophagus. Inside the proboscis the groove
becomes a crescentric chamber surrounding the mouth
(Figure 2F); the mouth opens at the tip of the muscular
pharyngeal mass. Salivary gland ducts attach to the outer
surface of the muscular pharyngeal mass (Figure 2G) and
empty at its distal end. Internally the pharyngeal mass is
divided into a tripartite food canal which is continuous
proximally with the thin-walled esophagus (Figure 2H).

Strands of host cells converge at the end of the proboscis
(Figure 2B). These cells appear to originate from both the

Page 344 The Veliger, Vol. 30, No. 4

Figure 2

Photomicrographs of Linckia laevigata arms with and without (Figure 2C) attachment or penetration by the snail
Thyca crystallina. A. A section through an entire snail and a fragment of a seastar arm at the level where the
proboscis penetrates the perihemal sinus. The section is oriented with the ambulacrum (a) on the lower side and

D. A. Egloff et al., 1988

host’s body wall surrounding the distal end of the proboscis
and from hemal tissue. The contents of the esophagus,
although sparse in sectioned specimens, occasionally in-
clude nuclei of cells in addition to larger quantities of
amorphous material.

DISCUSSION

The route of penetration of the proboscis of the female
Thyca crystallina into Linckia laevigata suggests that suf-
ficient food is available from some combination of hemal,
perihemal, and surrounding fluids and tissues to sustain
the ectoparasitic snail. This deduction is based on the fact
that the proboscis of large snails cannot be withdrawn
because the attachment disc is fused with the tissue of the
host and the fact that the proboscis has access to no other
sources of nutrients inside the host.

Alternative routes are possible but not utilized. For ex-
ample, holes in the body wall occupied by papulae (Figure
1), provide a short and direct access to the perivisceral
coelom, but in no specimens we examined did the proboscis
of Thyca crystallina take this path. Instead, the proboscis
bypasses the perivisceral coelom and proceeds deeper into
the host. This penetration must require extensive digestion
of dense dermal tissue and dissolution of calcareous ossi-
cles. The energetic costs of creating this circuitous route
to the hemal-perihemal complex ultimately must be more
than offset by a flow of nutrients to the snail.

The tissues of the host at the site of penetration are not
grossly injured; in fact, the opposite appears to be the case.
The region at the end of the proboscis has an abundance
of cells derived from the host’s body wall and from hemal
tissue. This suggests that the host is capable of replacing
the apparent loss of cells to the snail.

Thyca crystallina presumably shuns the more spacious
perivisceral coelom in favor of the relatively small hemal-
perihemal complex because the latter is a more concen-
trated source of nutrients than is the perivisceral coelom
(FERGUSON, 1982; BEIJNINK & VoocT, 1984). This hy-
pothesis is consistent with the observations in another as-
teroid, Echinaster graminicolus, where a radioisotopic tracer
appeared within 12-24 h in the ambulacral radial hemal

Page 345

tissue after injection of C'+-labeled amino acids (FERGUSON,
1970) or after feeding C'*-labeled clams or liquid glucose-
amino acid medium (FERGUSON, 1984). The proteins, gly-
coproteins, and possibly glycolipids stored in the hemal
strand of Asterias rubens (BEIJNINK & VOoGT, 1986) would
provide a rich source of complex nutrients for 7. crystallina
if present in Linckia laevigata.

In addition, the snail may be obtaining soluble food
produced at remote sites and transported to the snail through
the perihemal sinuses. The presence of flagellated cells in
the perihemal sinus (CUENOT, 1948; WALKER, 1979) of
some asteroids provides a means of moving nutrients in
solution through this system. Based on these observations,
FERGUSON (1984) concluded that nutritive metabolites are
translocated by some combination of movement and storage
within the hemal-perihemal complex.

Given the reported anatomical relationships and the
probable role of the hemal-perihemal complex in nutrient
transport and storage in asteroids, the stage is set for an
experimental determination of the kinds and rates of nu-
trient transfer through the hemal-perihemal complex of
Linckia laevigata by using Thyca crystallina as a natural
probe.

ACKNOWLEDGMENTS

Field work in 1965 was done by the first author while a
participant on Stanford University’s Ze Vega Cruise #7
supported by N.S.F. G17465. Laboratory work in 1978
was supported by Oberlin College Research and Devel-
opment Committee. We gratefully acknowledge the 1970
collections by the late Alan Banner and the advice and
encouragement of Charles Walker and Matthew Wilks.

LITERATURE CITED

ApDAM, W. 1934. Prosobranches parasites. Mem. Mus. Roy.
Hist. Natur. Belg. 2(14):87-115.

ANDERSON, J. M. 1966. Aspects of nutritional physiology. Pp.
329-357. In: R. A. Boolootian (ed.), Physiology of Echi-
nodermata. Interscience Publishers: New York.

BEIJNINK, F. B. & P. A. VoocT. 1984. Nutrient translocation
in the sea star: whole-body and microautoradiography after

ampulla (am) in the perivisceral coelom on the upper side. The left (L) and right (R) sides of the snail are indicated.
B. Higher magnification of the section in Figure 2A at the distal end of the proboscis (p), which encloses the
pharyngeal mass (m). The radial water canal (w), hemal tissue and associated perihemal sinuses (ph) lie above the
radial nerve (n). C. A section of an uninfected part of the same seastar arm proximal to the section shown in
Figures 2A, B. D. Section through the proboscis of another specimen showing the extent of the muscular pharyngeal
mass (m) in the proboscis (p). Lines (e-h) indicate the level of cross sections through the proboscis of a third
specimen shown in Figures 2E, F, G and H, respectively. E. Section of the proboscis (p) distal to the pharyngeal
mass and mouth. The groove in the proboscis appears to surround hemal tissue lying aborally to the radial nerve
(n) of the seastar. F. Section through the proboscis (p) at the point where the mouth (0) opens into the pharyngeal
mass. G. Section through the middle region of the muscular pharyngeal mass (m). Ducts (d) of the salivary gland
adhere closely to the outer edge of the pharyngeal mass. H. Section proximal to the pharyngeal mass showing the
esophagus (s) and the ducts of the salivary gland (d). Scale bars: A, 1 mm; B-D, 0.5 mm, E, 0.1 mm (the same

scale applies to F-H).

Page 346

ingestion of radiolabeled leucine and palmitic acid. Biol.
Bull. 166:669-682.

BEIJNINK, F. B. & P. A. VoocGT. 1986. The aboral haemal
system of the sea star, Asterzas rubens (Echinodermata, As-
teroidea): an ultrastructural and histochemical study. Zoo-
morphology 106:49-60.

BINYON, J. 1972. Physiology of echinoderms. Pergamon Press:
Oxford. 264 pp.

CHENG, T.C. 1964. The biology of animal parasites. Saunders
Company: Philadelphia. 727 pp.

CuENOT, L. 1948. Anatomie, éethologie et systématiques des
Echinodermes. In: P. P. Grassé (ed.), Traité de zoologie 11:
3-275. Masson: Paris.

ELperR, H. Y. 1979. Studies on the host parasite relationship
between the parasitic prosobranch Thyca crystallina and the
asteroid starfish Linckia laevigata. Jour. Zool. (Lond.) 187:
369-391.

FERGUSON, J. C. 1969. Feeding, digestion and nutrition in
Echinodermata. Pp. 71-100. Jn: M. Florkin & B. T. Scheer
(eds.), Chemical zoology. Vol. III. Echinodermata, Nema-
toda, and Acanthocephala. Academic Press: New York.

FERGUSON, J.C. 1970. An autoradiographic study of the trans-
location and utilization of amino acids by starfish. Biol. Bull.
138:14-25.

The Veliger, Vol. 30, No. 4

FERGUSON, J. C. 1982. Nutrient translocation. Pp. 373-393.
In: M. Jangoux & J. M. Lawrence (eds.), Echinoderm nu-
trition. Balkema: Rotterdam.

FERGUSON, J.C. 1984. Translocative functions of the enigmatic
organs of starfish—the axial organ, hemal vessels, Tiede-
mann’s bodies, and rectal caeca: an autoradiographic study.
Biol. Bull. 166:140-155.

Hyman, L. 1955. The invertebrates. Vol. IV. Echinodermata.
McGraw-Hill Book Company: New York. 763 pp.

KOEHLER, R. & C. VANEY. 1912. Nouvelles formes de Gas-
teropodes ectoparasites. Bull. Sci. Fr. Belg. 46:191-217.

KUKENTHAL, W. 1897. Parasitische Schnecken. Abh. Schneck-
enbergishen Ges. 24:1-14.

SARASIN, P. & F. SARASIN. 1887. Ueber zwei parasitische
Schnecken. Ergeb. Naturwiss. Forsch. Ceylon 1:1-32.
TayLor, J. D. & M.S. Lewis. 1970. The flora, fauna and
sediments of the marine grass beds of Mahe, Seychelles.

Jour. Natur. Hist. 4:199-220.

WALKER, C. W. 1979. Ultrastructure of the somatic portion of
the gonads in Asteroids, with emphasis on flagellated-collar
cells and nutrient transport. Jour. Morphol. 162:127-162.

YONGE, C. M. & T. E. THompson. 1976. Living marine mol-
luscs. Collins: London. 288 pp.

The Veliger 30(4):347-350 (April 1, 1988)

THE VELIGER
© CMS, Inc., 1988

Gastric Contents of /issurella maxima
(Mollusca: Archeogastropoda) at Los Vilos, Chile

CECILIA OSORIO

Departamento de Ciencias Ecologicas, Facultad de Ciencias, Universidad de Chile,
Casilla 653, Santiago, Chile

M. ELIANA RAMIREZ

Seccion Botanica, Museo Nacional de Historia Natural, Casilla 787, Santiago, Chile

JENNIE SALGADO

Departamento de Ciencias Ecologicas, Facultad de Ciencias, Universidad de Chile,
Casilla 653, Santiago, Chile

Abstract. The study of the gastric contents in 92 specimens of Fissurella maxima from Los Vilos,
Chile (31°51'S, 71°32'W) showed the presence of partially digested algal remains of 13 species. Diatoms
were present, as were whole animals. The macroalgae Chondrus, Gelidium, and Ulva, found throughout
the 13-month study period, had the greatest relative abundance in gastric contents. Other macroalgae
were occasionally present, with wide fluctuations in abundance; still others were recorded only once.
The analysis of the feces of keyhole limpets maintained in an aquarium showed abundant undigested
diatoms and remains of digested Gelidium and Porphyra which had been given as food. We conclude
that F. maxima is mainly a primary consumer which grazes on macroalgae in the rocky intertidal zone.

INTRODUCTION

Fissurella maxima Sowerby, 1835, is found on intertidal
rocks from Huarmey in Peru to Lirquen (Concepcion) in
Chile (McLean, 1984). Like other keyhole limpets, this
one is an important economic resource in Chile. Extraction
in 1985 was 3.653 tons and in 1986 was 2.159 tons
(ANUARIO ESTADISTICO DE PEsSCA, 1986).

Data available on Fissurella maxima include taxonomic
aspects (OsoRIO ef al., 1979; MCLEAN, 1984), age and
growth (BRETOS, 1982) and the reproductive cycle (BRETOS
et al., 1983; HERRERA, 1983; Aviles & Osorio, unpublished
data). There are no data in the literature on the feeding
habits of F. maxima. Such information would be essential
for the knowledge of the trophic position of the species and
its interactions with other intertidal organisms. Several
authors (e.g, MORENO & JARAMILLO, 1983; JARA &
MORENO, 1984; SANTELICES ef al., 1986; OLIVA & CASTI-
LLA, 1986) consider that the action of certain herbivorous
gastropods—trophic generalists of large body size—could
influence the abundance and species composition of inter-
tidal algal communities.

To document its feeding habits, we have analyzed the
stomach contents of Fissurella maxima during a 13-month
period in the intertidal zone of a northern Central Chilean
beach.

MATERIALS anp METHODS

The study site was Caleta “El Nague” at Los Vilos (31°51’S,
71°32'W). For the gastric analysis, 92 specimens of Fis-
surella maxima were collected, 6-8 specimens monthly,
with sizes ranging from 85 to 139 mm (reproductive size);
only five collected individuals were smaller than 85 mm.
Samplings were conducted from March 1983 through
March 1984.

Specimens collected were immediately injected with for-
malin in seawater in order to stop digestion. In the labo-
ratory, the stomach contents were emptied into a glass
cylinder and the total volume was measured. For analysis,
4 mL of the contents per stomach were used, 7.e., about
50% of the total volume. When the volume was under 4
mL, the total content of the stomach was analyzed. Indi-
vidual food items were separated under the microscope and

Page 348

their presence recorded. Histological sections were made
in order to identify the algal remains. The total volume
per month of each algal item was quantified by measuring
its volume displacement in a 1.25-mL cylinder graduated
to 0.25 mL. Values were expressed as the percentage of
relative abundance of each item in the total sample.

Feces of specimens kept in an aquarium were analyzed
under the microscope in order to determine whether dia-
toms were digested. Some keyhole limpets survived for 3
months in the aquarium. During this time they were fed
Porphyra and Gelidium.

RESULTS

All of the 92 examined stomachs contained algal and mi-
croalgal remains. In general the diet did not vary with
size. The gastric contents of the five individuals smaller
than 85 mm did not differ from those of the larger sizes.
Animal remains were found only occasionally. The mi-
croalgal genera most frequently found were diatoms of
several genera: Synedra, Lichmophora, Thalasswosira, Coc-
coneis, Pleurosigma, and Coscinodiscus. Diatoms did not
show signs of digestion.

Among the animals were small crustaceans (copepods
and cypris larvae), a few gastropods, bivalve post-larvae,
and two individuals each of polychaetes and medusae. It
is worth noting that these animals showed no signs of
trituration or digestion.

Macroalgae were abundant and, unlike the former
groups, they showed clear evidence of digestion. Thirteen
species were found: Chondrus canaliculatus (C. Ag.) Grev.,
Glossophora kunthu (C. Ag.) J. Ag., Halopteris funicularis
(Mont.) Sauv., Corallina officinalis var. chilensis (Dec.)
Kutz., Lessonia nigrescens Bory, Codium dimorphum Sve-
delius, Adenocystis utricularis (Bory), Porphyra columbina
Mont., Pterosiphonia dendroidea (Mont.) Salk., Gelidium
sp., Ulva sp., Cladophora sp., and Enteromorpha sp. Of
these, nine species were present in considerable amounts
and could be quantified.

Chondrus, Gelidium, and Ulva were found throughout the
13 months of sampling, being present in 71%, 70%, and
54% of the examined stomachs respectively. Glossophora,
Halopteris, Cladophora, Corallina, and Lessonia were pres-
ent for at least 8 months. Codiwm, Adenocystis, and Porphyra
occurred during only 4 months. In terms of relative abun-
dance, the most important genera were Chondrus, Gelid-
wm, Ulva, and Glossophora, the total volumes of which
added up to 80%.

The monthly variation of the most frequently found
algae, arranged by major taxa, is represented in Figure 1.
The most abundant Rhodophyta were Chondrus and Gel-
idium (Figure 1a). Chondrus exhibited high values from
May through October, with maximum abundance in Au-
gust (62.5%). On the other hand Gelidium showed higher
variations in abundance than Chondrus, with two peaks,
one in September (50%) and another in December (45.4%).

Phaeophyta were less abundant (Figure 1B) and their

The Veliger, Vol. 30, No. 4

maximum values reached only 30%. In this group, Glos-
sophora and Halopteris were the most abundant, but with
discontinuous values during the year.

Among the Chlorophyta, Ulva was recorded the year
round with maximum abundance in March 1983 and
March 1984 (29.4% and 33.3% respectively). The values
for Ulva were markedly lower from August to December.
Cladophora appeared somewhat irregularly with maximal
abundance from November to January.

The analysis of the trophic spectrum per month disclosed
that Mssurella maxima ingests simultaneously from 5 to 10
macroalgal species, with variable abundance throughout
the year. The largest variety was observed in summer—
January, February—with 9 or 10 species, whereas in June,
November, and December only 5 algal species were re-
corded as food items. All the remaining species of mac-
roalgae showed wide temporal fluctuations in abundance,
particularly Corallina, Lessonia, Codium, Adenocystis, and
Porphyra. Two algae were recorded only once during the
study period: Pterosiphonia (March 1983) and Enteromor-
pha (August 1983).

The specimens maintained in the aquarium fed at night,
and no apparent activity was recorded during the day. The
analysis of the feces obtained during the first six days
revealed abundant diatoms (Lichmophora, Synedra, Navic-
ula, Grammatophora, Amphora, Cocconeis, Nitzchia, C'ym-
bella, Ceratoneis, Entophyla, Rhabdonema, Rhoicosphema,
Pleurosigma, Coscinodiscus, and Pinnularia) with no signs
of digestion; thecae and chloroplasts were still present.
Feces after 30 and 60 days contained only scarce diatoms
(Cocconeis, Pinnularia, and Grammatophora) and residues

of Gelidium and Porphyra, which had been fully digested.

DISCUSSION

The diet of Fissurella maxima at Caleta El Nague in Los
Vilos consisted mostly of macroalgae. Other organisms
such as diatoms, seemed to be less important in nutrition,
since they may have passed through the gut undigested.
They were probably passively ingested with the macro-
algae.

Fissurella maxima seems to be a generalist herbivore
feeding especially on Chondrus, Gelidium, and Ulva. Oc-
casionally it consumes other algae such as Corallina, Les-
sonia, Codium, Adenocystis, and Porphyra. Another keyhole
limpet, Fissurella crassa Lamarck, 1822, is also a generalist
herbivore whose diet at a nearby site in Pelancura (33°35’S,
71°38'W), between April 1983 and April 1984, consisted
of microalgae, macroalgae (ulvoids, Schottera, Gelidium,
and calcareous algae), invertebrate remains, and spores
(SANTELICES et al., 1986). However, the diets of the two
species seem to differ in their composition. Such differences
could be related to the ecological distributions of the two
Fissurella species. Fissurella maxima inhabits the low in-
tertidal zone, while F. crassa is mostly found on the upper
intertidal zone, where it reaches higher levels than other
keyhole limpets (MCLEAN, 1984). On the other hand F.

C. Osorio et al., 1988

60 fA

40

Page 349

Rhodophyta

O Gelidium
@® Chondrus

40

3
=, 20
3
ie)
>
©
40
20

MA M J J
1983

Figure 1

AE Sie OheNi OU ba aM

Phaeophyta

@ Glossophora
O Halopteris

Chlorophyta

A Ulva
A Cladophora

Month

1984

Monthly variation of the main algae in the gastric contents of Fisswrella maxima at Los Vilos, Chile, from March

1983 to March 1984.

barbadensis (Gmelin, 1791), found in Barbados (WARD,
1966), has been reported to ingest preferably green and
blue-green algae, sand grains, diatoms, small crustaceans,
bivalves, and occasionally Foraminifera. The only food
items this species seems to share with F. maxima are Cla-
dophora and Ulva. These differences in diet could be ex-
plained by the different ecological conditions of their hab-
itats.

The variations in relative abundances of algae in the
stomach contents may or may not relate to the relative
abundances of algae in the community. For example, 12
species of the macroalgae identified in the stomachs of
Fissurella maxima are known to occur the year round in
the rocky intertidal zone of central Chile (SANTELICES &
VERA, 1984). However, without more detailed knowledge
of the relative abundances we cannot ascertain preferences
in this keyhole limpet.

SANTELICES (1981) suggests that Codiwm and Gelidium
may escape herbivory owing to their growth patterns, which

result in a continuous cover. In turn, Lessonia and Corallina
may also escape predation, the former because of its large
size and the latter on account of its rough texture. However,
the presence of all these species in the stomach of Fissurella
maxima questions these hypotheses. Furthermore, STENECK
& WATLING (1982) consider that the rhipidoglossan radula
of F. maxima would not be adequate for grazing on rough
textured algae. The finding of Corallina in the stomach of
this species challenges this notion, and supports SANTE-
LICES et al. (1986) who suggest that the different shapes
of gastropod radulas do not necessarily relate to the kind
of algae ingested.

Based on its gastric contents, we conclude that Frssurella
maxima is ““euriphycophagous” and a primary consumer
of macroalgae in the rocky intertidal zone of Chile.

ACKNOWLEDGMENTS

The authors thank N. Bahamonde and D. Soto for valuable
suggestions and revision of the manuscript; V. Montecino

Page 350

for identifying diatoms; C. Fernandez for the diagrams
and M. Bustos for technical assistance; and two anonymous
reviewers for valuable suggestions.

This study was supported by Project N 1754-8522 of
the Departamento de Investigacion y Bibliotecas de la
Universidad de Chile.

LITERATURE CITED

ANUARIO ESTADISTICO DE PESscA. 1986. Servicio Nacional de
Pesca, Chile.

BretTos, M. 1982. Biologia de Fissurella maxima (Moll; Ar-
chaeogastropoda) en el norte de Chile I. Caracteres gene-
rales, edad y crecimiento. Cahiers Biol. Mar. 23:159-170.

BretTos, M., I. TESORIERI & L. ALVAREZ. 1983. The biology
of F. maxima in northern Chile. II. Notes on its reproduction.
Biol. Bull. 165:559-568.

HERRERA, G. 1983. Analisis estacional del ciclo sexual en ovario
de F. maxima en el norte de Chile. Resumen, Reunion Soc.
Biol. 1983.

Jara, F. H. & C. Moreno. 1984. Herbivory and structure in
a midlittoral, rocky community: a case in southern Chile.
Ecology 65:28-38.

McLean, J. 1984. Systematics of Fissurel/a in the Peruvian
and Magellanic faunal provinces (Gastropoda: Prosobran-
chia). Contribution in Science No. 354:1-70. Natur. Hist.
Mus. Los Angeles.

The Veliger, Vol. 30, No. 4

Moreno, A. C. & E. JARAMILLO. 1983. The role of grazers
in the zonation of intertidal macroalgae of the Chilean coast
near Valdivia. Oikos 41:73-76.

Ouiva, D. & J. C. CasTILLa. 1986. The effect of human ex-
clusion on the population structure of key-hole limpets Fis-
surella crassa and F. limbata on the coast of central Chile.
Mar. Ecol. 7(3):201-217.

Osorio, C., J. ATRIA & S. MANN. 1979. Moluscos marinos de
importancia economica en Chile. Biol. Pesq. 11:3-47.
SANTELICES, B. 1981. Perspectivas de investigacion en estruc-
tura y dinamica de comunidades intermareales rocosas de
Chile central. I. Cinturones de macroalgas. Medio Ambiente

5(1-2):175-189.

SANTELICES, B., J. VASQUEZ & I. MENESES. 1986. Patrones de
distribucion y dietas de un gremio de moluscos herbivoros
en habitats intermareales expuestos de Chile central. Mono-
grafias Biologicas 4:147-171.

SANTELICES, B. & M. E. VERA. 1984. Variacion estacional de
floras marinas en Caleta Horcon, Chile central. Phycol. Lat.
Amer. 2:83-101.

STENECK, R.S. & L. WATLING. 1982. Feeding capabilities and
limitations of herbivorous molluscs: a functional group ap-
proach. Mar. Biol. 68:299-319.

WaRD, J. 1966. Feeding, digestion and histology of the digestive
tract in the key hole limpet Fissurella barbadensis Gmelin.
Bull. Mar. Sci. 16(4):668-683.

The Veliger 30(4):351-357 (April 1, 1988)

THE VELIGER
© CMS, Inc., 1988

Variable Population Structure and ‘Tenacity in the

Intertidal Chiton Katharina tunicata

(Mollusca: Polyplacophora) in Northern California

by

TIMOTHY D. STEBBINS

Department of Biological Sciences, University of Southern California,
Los Angeles, California 90089, U.S.A. and
Invertebrate Zoology Section, Los Angeles County Museum of Natural History,
Los Angeles, California 90007, U.S.A.

Abstract.

Populations of the chiton Katharina tunicata (Wood, 1815) were studied at three rocky

intertidal areas in northern California, each subjected to a different degree of wave exposure. The spatial
density and size structure of Katharina populations varied with the degree of exposure to wave action.
Chiton densities increased and body sizes decreased with increased exposure to wave action. Laboratory
experiments showed that tenacity (adhesion strength, or resistance to shear force) of Katharina signifi-
cantly increased with a decrease in body size. This increased capacity of smaller chitons to resist removal
from the substratum may provide a mechanism for the observed patterns of abundance and size-

distribution of Katharina.

INTRODUCTION

Organisms living in rocky intertidal areas on exposed shores
encounter a number of biological and environmental fac-
tors that interact to regulate population and community
structure (see reviews by CONNELL, 1972; STEPHENSON &
STEPHENSON, 1972; RICKETTS ef al., 1985). Waves are an
important agent of disturbance on rocky shores and may
be extremely important in structuring intertidal popula-
tions and communities (e.g., JONES & DEMETROPOULOS,
1968; PAINE & LEVIN, 1981; DENNY, 1985; DENNY et ai.,
1985). Analyses of intraspecific variation of important in-
tertidal organisms at sites varying in exposure may yield
information critical to our understanding of community
ecology.

Chitons are conspicuous components of intertidal com-
munities in many areas of the world (BOYLE, 1970; GLYNN,
1970; PAINE, 1980; DETHIER & DUGGINS, 1984; DUGGINS
& DETHIER, 1985; OTAIZA & SANTELICES, 1985). The
role of motile herbivores like chitons in regulating algal
composition and ultimately community structure may be
extremely important (PAINE & VADAS, 1969; DayTon,
1975; LUBCHENCO & MENGE, 1978; LUBCHENCO &
GAINES, 1981). Aside from studies on reproductive biology
(HIMMELMAN, 1978, 1979, 1980; PEARSE, 1978; SAKKER,

1986) relatively little is known about the ecology of inter-
tidal chitons (see BOYLE, 1970; GLYNN, 1970; ANDRUS &
LEGARD, 1975; DETHIER & DUGGINS, 1984; DUGGINS &
DETHIER, 1985; OTAIZA & SANTELICES, 1985).

The chiton Katharina tunicata (Wood, 1815) (hereafter
as Katharina) is an important member of mid- to low-
intertidal communities along the Pacific coast of North
America (HIMMELMAN, 1978; DETHIER & DUGGINS, 1984;
DuGoGIns & DETHIER, 1985), and has a geographic range
from Alaska to southern California (HADERLIE & ABBOTT,
1980; RICKETTS et al., 1985). Despite the abundance and
importance of Katharina in structuring intertidal com-
munities (DETHIER & DUGGINS, 1984; DUGGINS & DE-
THIER, 1985) little is known regarding intraspecific vari-
ation in this chiton.

Preliminary observations suggested that the population
structure of Katharina varied at different sites in northern
California. In this study abundances and size distributions
of Katharina were quantified at three rocky intertidal areas
and correlated with the degree of wave exposure at the
sites. In addition, the tenacity (adhesion strength) of chi-
tons was measured in the laboratory to determine if te-
nacity varied with body size. Finally, several alternative
hypotheses are discussed that may explain the observed
patterns of Katharina population structure.

Page 352

PACIFIC
OCEAN

Figure 1

Location of study areas (arrows) near Trinidad, northern Cal-
ifornia (41°03'07"N, 124°07'51”W). In order of decreasing ex-
posure to wave action the study sites are Trinidad State Beach,
College Cove, and Trinidad Bay.

MATERIALS anD METHODS
Study Areas

The study was conducted at three rocky intertidal areas
near Trinidad, in northern California (Figure 1). The sites
were similar in terms of inclination and heterogeneity of
the substratum and were covered primarily with crustose
coralline algae and clumps of the laminarian Hedophyllum
sessile (C. Agardh) Setchell. Katharina tunicata was the
most prominent herbivore at the sites, although the limpets
Lottia pelta (Rathke, 1833) (=Collisella pelta) and Tectura
scutum (Rathke, 1833) (=Notoacmea scutum) were also
common. The seastar Pisaster ochraceus (Brandt, 1835)
occurred at all sites below the zone of Katharina, although
it was more abundant at the most exposed site.

Transects were initially established at each study site
through belts of Hedophyllum at about 0.5 m below to 0.5
m above mean lower low water. These transects were
oriented perpendicular to the direction of wave impact and
marked by permanent 5-cm? markers bolted to the sub-
stratum.

The three study areas differ in their degree of exposure
to wave action. Trinidad State Beach faces west-northwest

Table 1

Exposure indices at three study areas in northern Cali-
fornia from April 1980 to April 1981. Exposure index =
(no. of transect markers lost + no. of marker-months) x
100. A marker-month is one marker in place for 1 month.

Study area Exposure index
Trinidad State Beach 26.9 (7/26)
College Cove 13.8 (4/29)
Trinidad Bay 0 (0/36)

The Veliger, Vol. 30, No. 4

Weight
Container

Plexiglas

Figure 2

Apparatus used to measure tenacity of chitons on a hard substrate
(Plexiglas) and subjected to shear forces.

and receives the full force of waves and swells. College
Cove is slightly protected from wave action by a projecting
headland. The south-facing Trinidad Bay site is largely
protected from most waves and swells by Trinidad Head
and numerous offshore rocks. A more objective “exposure
index” similar to that described by MENGE (1976) was
calculated for each area (Table 1) and supported the sub-
jective observations. In order of decreasing exposure to
wave action, the study areas were Trinidad State Beach,
College Cove, and Trinidad Bay.

Sampling Procedures

Katharina populations were examined monthly at each
site over a 13-month period from April 1980 to April 1981,
except in January 1981 when severe wave action prohib-
ited access. Monthly population densities and size-class
distributions were estimated from 10 randomly chosen 0.25-
m?’ quadrats along the transects at each study site. All
chitons occurring within the quadrats were counted, and
body lengths measured to the nearest 0.1 mm with calipers.
Mean numbers of individuals per 0.25 m? and mean body
lengths were calculated monthly for each site.

Experimental Procedures

Sixty-four individuals of Katharina between 1.0 and 10.0
cm in body length were studied to determine if their ability
to resist removal from a hard substrate (defined as tenacity)
varied with body size. Chitons were collected near the field
sites between April and August 1981 and maintained in
running seawater aquaria at the Telonicher Marine Lab-
oratory (Trinidad, California) of Humboldt State Uni-
versity. All test specimens were used within 2 weeks of
collection and each animal was used in only one test. Only
healthy animals were tested. Tenacity, expressed as the
force per unit area required to dislodge a chiton, was
measured using an apparatus that applied a shear force
parallel to the chiton’s foot (Figure 2). Test substrates

T. D. Stebbins, 1988

=
{o)

TSB

cc
TB

MEAN NO. CHITONS / 0.25 m2
= YN OW AN ON © OO

AMJJASONODJS FMA
1980 1981
MONTH

Figure 3

Population densities of Katharina tunicata at Trinidad State Beach
(TSB), College Cove (CC), and Trinidad Bay (TB) in northern
California. Data for each month are expressed as mean number
of chitons per 0.25 m? + 1 SE.

were roughened Plexiglas discs 10 cm in diameter. Chitons
were allowed to remain attached to the test surface for
approximately 2 h prior to testing. After attachment, the
test disc was attached to the apparatus and the lever po-
sitioned parallel to the plane of the foot of the attached
chiton. Each individual was tapped lightly immediately
before testing to induce it to adhere to the substratum as
tightly as possible. Weights were then added to the con-
tainer in 25 g increments every 2.5 sec until the chiton
was dislodged from the surface; the maximum weight (g)
necessary to cause detachment was recorded. The body
length and weight of each individual were measured after
testing. The foot surface area (cm?) was determined by
placing the chiton on a transparent grid. Tenacity was
calculated as total weight applied per foot area, and con-
verted to newtons per m* (N-m_’).

RESULTS
Abundance and Size Distribution

The average numbers of Katharina per 0.25 m? were
plotted over the study period for each study site (Figure
3). These mean densities throughout the year differed sig-
nificantly between sites (P < 0.005; Kruskal-Wallis Anal-
ysis of Variance). The chiton densities at Trinidad Bay
were significantly lower than at College Cove and Trinidad
State Beach, and the densities at College Cove were sig-
nificantly lower than those at Trinidad State Beach (P <
0.001; Mann-Whitney U-test). The densities during the
study ranged from 0 to 16 chitons per 0.25 m?. The animals
tended to aggregate around and under clumps of Hedo-
phyllum, accounting for an observed patchiness. Generally
there were no significant seasonal trends in density fluc-
tuations. However, the decreases in Katharina densities

Page 353

10
eo
(5)
= 38
TB
ie tater tt PO
g
w 6
|
> > cc
4
srs
S12
=;

AMJJASONODJ FMA
1980 1981
MONTH

Figure 4

Mean body sizes of Katharina tunicata at Trinidad State Beach
(TSB), College Cove (CC), and Trinidad Bay (TB) in northern
California. Data for each month are expressed as mean body
length (cm) of chitons + 1 SE.

between December 1980 and February 1981 may be re-
lated to severe storm activity during that period.

The mean body lengths of Katharina were plotted for
each area over the study period (Figure 4) and were found
to differ significantly between sites (P < 0.001; one-way
ANOVA). Trinidad Bay chitons were significantly larger
than those at College Cove and Trinidad State Beach, and
the chitons at College Cove were significantly larger than
those at Trinidad State Beach (P < 0.05; Student-New-
man-Keuls test). The body lengths of individuals ranged
from 0.72 to 10.15 cm during the study with maximum
mean lengths occurring in May 1980 at all sites. The size-
class distributions clearly show the distinct nature of the
three Katharina populations (Figure 5). Greater than 70%
of the chitons at Trinidad State Beach, the most exposed
site, were consistently less than 5.0 cm in length, while
chitons in this size range consistently made up less than
20% of the population at the least exposed site, Trinidad
Bay. The size range of College Cove chitons was inter-
mediate between the two extreme sites.

Recruitment

Katharina grows to a length of 2.5 cm during its first
year (HYMAN, 1967). The relative frequency of juvenile
chitons less than 2.0 cm long was plotted for each site over
the study period and used as an estimate of recruitment
(Figure 6). From these data it appears that recruitment
differed significantly at the sites, at least immediately pre-
ceding and during this study. Juveniles of Katharina were
a conspicuous component of the chiton population through-
out the year at Trinidad State Beach, with a noticeable
peak following the summer of 1980. This peak corresponds
with a main spawning period in June as reported by HIM-

Page 354

TSB cc TB
40 APR
30
an 1980
MAY
JUN
JUL
S AUG
&
a
a SEP
Oo
a
WL
o
w OCT
(O)
<
Ee
4
Ww
rs} NOV
x
WW
a
DEC
FEB
1981
MAR
40
30 APR
20
10
0246810 0246810 02468 10

SIZE CLASS (cm)

Figure 5

Katharina tunicata. Size-frequency distributions of chitons at three
study areas in northern California: Trinidad State Beach (TSB),
College Cove (CC), and Trinidad Bay (TB).

MELMAN (1978). In contrast, juveniles were much rarer
at the other two study sites.

Juvenile Katharina occurred in five different microhab-
itats during low tides: (1) in cracks or crevices on exposed
surfaces, (2) in cracks or crevices under blades of Hedo-
phyllum, (3) on bare rock or coralline crusts under He-
dophyllum blades, (4) under adult Katharina, and (5) with-
in Hedophyllum holdfasts. Another chiton, Lepidochitona
dentiens (Gould, 1846) (=Cyanoplax dentiens), often co-
existed with Katharina juveniles within kelp holdfasts.

The Veliger, Vol. 30, No. 4

S
3 40
”
ai TSB
=> 30
oz
ug \
> oo
oS
a
m 10 TB
c A”

AMJJASONODJS EMA
1980 1981
MONTH

Figure 6

Recruitment of Katharina tunicata as estimated by the relative
frequency of juveniles (length < 2.0 cm) in chiton populations
at Trinidad State Beach (TSB), College Cove (CC), and Trinidad
Bay (TB).

Tenacity

There was a significant decrease of tenacity (N-m~?)
with increasing body size (P < 0.001; see Figure 7). Small
chitons (2-3 cm long) were up to twice as resistant to
removal as were large individuals (8-10 cm). Resistance
of animals ranged from 0.87 x 10* N-m~ (a 9.31 cm
individual) to 5.10 x 10* N-m~? (a 2.16 cm individual
and a 2.49 cm individual). Mean tenacity for all Katharina
tested (n = 64) was 2.45 + 1.00 x 10* N-m~? (x + SD).
LINSENMEYER (1975) reported a lower mean resistance
value for Katharina equivalent to 1.45 + 0.38 x 104
N-m~? (nm = 12); however, he provided no data on body
sizes. Linsenmeyer’s tower value may simply reflect his
use of larger individuals.

DISCUSSION

Katharina tunicata 1s a major determinant of intertidal com-
munity structure in the eastern North Pacific whose im-
portance stems from its size, density, and generalist feeding
behavior (DETHIER & DUGGINS, 1984; DUGGINS & DE-
THIER, 1985). However, little is known regarding variation
between populations of this chiton. Katharina was the dom-
inant herbivore at my study sites, averaging approximately
10-36 individuals per m?. These densities are comparable
to those described for more northern populations (PAINE,
1980; DETHIER & DUGGINS, 1984; DUGGINS & DETHIER,
1985). The density and size structure of Katharina pop-
ulations were shown to vary with the degree of exposure
to wave action (Figures 3-5). There was an inverse cor-
relation between population densities and body size of
chitons at the three study sites; density increased and body
size decreased with increased exposure to wave action.

T. D. Stebbins, 1988

Page 355

ANDRUS & LEGARD (1975) reported similar observations
for Katharina in central California. Similar patterns of
abundance and size distribution have been reported for
other motile invertebrates including limpets in Great Brit-
ain (JONES, 1948; SOUTHWARD, 1953; SOUTHWARD &
ORTON, 1954; BALLANTINE, 1961) and Australia (MEYER
& O’GowWER, 1963). HARGER (1970, 1972) and PAINE
(1976a, b) have shown that temperate mussels and seastars
also increase in size where wave action is less, while
CONNELL (1972) has shown a similar trend for some ma-
rine algae. In contrast, OTAIZA & SANTELICES (1985) re-
ported that the large Chilean chitons Acanthopleura echi-
nata (Barnes, 1824) and Chiton latus Sowerby, 1825,
displayed an opposite trend, with larger individuals oc-
curring in the most exposed habitats.

Patterns of intertidal population and community struc-
ture are the result of complex interactions of predation,
competition, biological disturbance, exposure to wave ac-
tion, and the inclination and heterogeneity of the substra-
tum (DayTon, 1971; MENGE, 1976). The inclination and
heterogeneity of the substratum were similar at my three
northern California study sites and were probably not
responsible for differences between Katharina populations.
Intraspecific competition was probably not important since
neither food nor space ever appeared to be limiting. In-
terspecific competition was probably minor since no major
competitors for the large macrophytic algae (e.g., Hedo-
phyllum) occurred in these areas. The only other common
herbivores at these sites were the limpets Lottia pelta and
Tectura scutum. These limpets have been described as “in-
direct commensals” of Katharina (DETHIER & DUGGINS,
1984) and probably have little effect on chiton population
structure. Predation pressure may vary between sites since
the predatory seastar Pisaster ochraceus was more abundant
at the most exposed site, Trinidad State Beach. Although
Pisaster is known to eat Katharina (PAINE, 1966; DAYTON,
1975; CAREFOOT, 1977), I never noticed an instance of
predation in three years of observation. Thus, it seems
unlikely that seastar predation plays a major role in reg-
ulating chiton populations near Trinidad, although these
observations were restricted to periods of low tides. More
information on the feeding habits of Prsaster during high
tides is needed before definitive conclusions can be made
regarding the effect of predation on Katharina.

Many motile invertebrates (e.g., seastars, limpets, and
chitons) can withstand the direct force of waves by adhering
tenaciously to the substratum. The effects of wave action
on populations of these organisms cannot be easily pre-
dicted. However, degree of wave action may have impor-
tant consequences on the age or size structure of intertidal
populations, since waves are more likely to remove large
than small individuals from the substratum (DENNY et al.,
1985). Larger chitons may have a greater likelihood of
being detached because, as body length increases, the area
of attachment (7.e., the foot) does not increase proportion-
ately. Consequently, large animals have a greater ratio of

6 86 8

8

TENACITY (N/m?- 103)
3

1 2 3 4 5 6 7 8 9
BODY LENGTH (cm)

Figure 7

Tenacity of Katharina tunicata. Resistance of chitons on a hard
substrate (Plexiglas) to removal by a shear force. Least-squares
linear regression of tenacity (N-m~’) as a function of body size
(length in cm). Regression line (y = 45418 — 3576x) significant
at P < 0.001 (n = 64).

body size to attachment surface and higher profile than
small individuals, and could be more susceptible to de-
tachment by wave action. If such is the case, wave action
could regulate Katharina population structure by removing
larger animals in greater numbers than small animals. If
this hypothesis is correct, one would expect large chitons
to be less abundant than small individuals at areas of high
wave impact, and more abundant at more protected areas.
Such was the case at the northern California sites. These
observations suggest that small chitons have an advantage
over large individuals at withstanding forces associated
with wave shock. Although LINSENMEYER (1975) dem-
onstrated that the force required to dislodge different species
of chitons was directly related to the degree of wave action
in the habitat of each species, no attempt was made to
determine if resistance to removal (tenacity) varied with
body size.

In this study, there was a significant relationship be-
tween the body size and tenacity of Katharina; tenacity
increased with decreased body size (Figure 7). This in-
creased capacity of smaller chitions to resist removal from
the substrate may explain the observed patterns of abun-
dance and size distribution of these animals near Trinidad,
by way of limiting the size of chitons at more exposed
areas. Although this differential size resistance may ex-
plain the observed population structure of Katharina, this
hypothesis depends upon several assumptions. First, the
adhesive abilities of Katharina will limit populations only
if chitons actually are washed off the substrate. At present
there is no direct evidence that they are. Secondly, the
chitons must experience shear forces near their adhesive
strengths if they are going to be dislodged. This is difficult
to determine for Katharina because tenacity values were
calculated using an unnaturally smooth substrate (Plexi-
glas), and therefore probably represent underestimates of

Page 356

this chiton’s true adhesive abilities (see MILLER, 1974;
LINSENMEYER, 1975; DENNY et al., 1985). Furthermore,
chitons may not adhere in the lab with a tenacity ap-
proaching that in nature. However, these estimates of
Katharina tenacity (~1-5 x 10* N-m~*) are only an order
of magnitude lower than values for limpets (~1-4 x 105
N-m~?) (BRANCH & Mars, 1978; GRENON & WALKER,
1982; DENNY et al., 1985) on natural surfaces. It seems
likely that Katharina has adhesive strength at least com-
parable to limpets under natural conditions. DENNY et al.
(1985) and others have concluded that, at least for limpets,
adhesion is much stronger than typical wave shear. In
addition, GLYNN (1970) reported that the Caribbean chi-
tons Acanthopleura granulata (Gmelin, 1791) and Chiton
tuberculatus Linnaeus, 1758, were capable of surviving
forces equivalent to those generated by waves 5.5 m high.
Finally, there is evidence that normal (lift) forces may be
more important than the shear forces measured here
(DENNY et al., 1985).

Although the size-resistance hypothesis may explain the
observed patterns of abundance and size distribution of
Katharina, several other alternative hypotheses also explain
these patterns. (1) Topographic irregularities (e.g., holes
and crevices) may provide greater refuge from wave impact
to small chitons than large individuals; large chitons would
be selectively removed from areas of high wave impact
owing to the lack of suitable refuge. The restriction of
juvenile Katharina to some type of shelter (under kelp or
adult chitons, in cracks or crevices) lends support to this
hypothesis. (2) Differential recruitment may be important.
Increased recruitment rates at areas at high wave exposure
could explain the observed patterns. However, these pat-
terns may be variable in time and space and have little to
do with the sites themselves. (3) Less feeding time at areas
of high wave impact, due to the increased turbulence in
these areas, could cause lower growth rates in chitons;
these lower growth rates could result in smaller individuals
at areas of high wave exposure. (4) The reduced body size
of chitons at areas of high wave shock may be due to
increased mortality rates (decreased mean longevity) as-
sociated with the severity of the environment.

Knowledge of intraspecific variation of important in-
tertidal species is essential to developing a clear under-
standing of community organization and structure. More
data on chiton hydrodynamics and on feeding times, re-
cruitment, growth rates, and longevity for Katharina at
areas of varied exposure to wave action are needed to
interpret adequately the role that various factors play in
regulating the population structure of this animal. Wave
action may mediate the population structure of this chiton
through complex interactions of some or all of the above
proposed hypotheses.

ACKNOWLEDGMENTS

I wish to thank Drs. M. J. Boyd and G. J. Brusca for
their advice and guidance throughout this project. I grate-

The Veliger, Vol. 30, No. 4

fully acknowledge: P. Bixler, L. Bott, K. Cooper, G. Cran-
dell, C. Diebel, V. Frey, R. Rasmussen, and D. Richards
for discussions; P. Collins for computer advice; and R.
Holsinger for design and construction of the tenacity ap-
paratus. The director and staff of the Telonicher Marine
Laboratory kindly provided use of their facilities. I am
deeply indebted to P. Bixler, S. Birks, and Jesse for field
assistance. This manuscript benefitted substantially from
critical reviews by G. J. Bakus, M. J. Boyd, G. J. Brusca,
R. C. Brusca, P. M. Delaney, M. W. Denny, and J. F.
Quinn. This work is based in part on a M.A. Thesis
submitted to the Department of Biological Sciences at
Humboldt State University, California.

LITERATURE CITED

ANpbRUus, J. K. & W. B. LeGaRD. 1975. Description of the
habitats of several intertidal chitons (Mollusca: Polyplaco-
phora) found along the Monterey Peninsula of central Cal-
ifornia. Veliger 18(Suppl.):3-8.

BALLANTINE, W. J. 1961. A biologically-defined exposure scale
for the comparative description of rocky shores. Field Studies
1:1-19.

Boye, P. R. 1970. Aspects of the ecology of a littoral chiton,
Spharochition pelliserpentis (Mollusca: Polyplacophora). N.Z.
Jour. Mar. Freshwater Res. 4:364-384.

BRANCH, G. M. & A. C. MarsH. 1978. Tenacity and shell
shape in six Patella species: adaptive features. Jour. Exp.
Mar. Biol. Ecol. 34:111-130.

CaREFOOT, T. H. 1977. Pacific seashores. A guide to intertidal
ecology. University Washington Press: Seattle. 208 pp.
CONNELL, J. H. 1972. Community interactions on marine rocky

intertidal shores. Ann. Rev. Ecol. Syst. 3:169-191.

DayTon, P. K. 1971. Competition, disturbance, and commu-
nity organization: the provision and subsequent utilization
of space in a rocky intertidal community. Ecol. Monogr. 41:
351-389.

Dayton, P. K. 1975. Experimental evaluation of ecological
dominance in a rocky intertidal algal community. Ecol.
Monogr. 45:137-159.

Denny, M. W. 1985. Wave forces on intertidal organisms: a
case study. Limnol. Oceanogr. 30:1171-1187.

Denny, M. W., T. L. DANIEL & M. A. R. KOEHL. 1985.
Mechanical limits to size in wave-swept organisms. Ecol.
Monogr. 55:69-102.

DETHIER, M. N. & D. O. Duceins. 1984. An “indirect com-
mensalism” between marine herbivores and the importance
of competitive hierarchies. Amer. Natur. 124:205-219.

Ducains, D.O. & M. N. DETHIER. 1985. Experimental stud-
ies of herbivory and algal competition in a low intertidal
habitat. Oecologia 67:183-191.

GLYNN, P. W. 1970. On the ecology of the Caribbean chitons
Acanthopleura granulata Gmelin and Chiton tuberculatus Lin-
née: density, mortality, feeding, reproduction, and growth.
Smithson. Contrib. Zool. 66:1-21.

GRENON, J.-F. & G. WALKER. 1982. The tenacity of the limpet
Patella vulgata L.: an experimental approach. Jour. Exp.
Mar. Biol. Ecol. 54:277-308.

HADERLIE, E. C. & D. P. ABBoTT. 1980. Polyplacophora: the
chitons. Pp. 412-428. In: R. H. Morris, D. P. Abbott & E.
C. Haderlie (eds.), Intertidal invertebrates of California.
Stanford Univ. Press: Stanford, California.

HarGER, J. R. E. 1970. The effect of wave impact on some
aspects of the biology of sea mussels. Veliger 2:401-414.

T. D. Stebbins, 1988

HarGe_r, J. R. E. 1972. Competitive coexistence: maintenance
of interacting associations of the sea mussels Mytilus edulis
and Mytilus californianus. Veliger 14:387-410.

HIMMELMAN, J. H. 1978. The reproductive cycle of Katharina
tunicata Wood and its controlling factors. Jour. Exp. Mar.
Biol. Ecol. 31:27-41.

HIMMELMAN, J. H. 1979. Factors regulating the reproductive
cycles of two northeast Pacific chitons, Tonicella lineata and
T. insignis. Mar. Biol. 50:215-225.

HIMMELMAN, J. H. 1980. Reproductive cycle patterns in the
chiton genus Mopalia (Polyplacophora). Nautilus 94:39-49.

HyMan, L. H. 1967. The invertebrates: volume VI, Mollusca
I. McGraw-Hill: New York. 792 pp.

Jones, N. S. 1948. Observations and experiments on the bi-
ology of Patella vulgata at Port St. Mary, Isle of Man. Proc.
Trans. Liverpool Biol. Soc. 56:60-77.

JONEs, W. E. & A. DEMETROPOULOS. 1968. Exposure to wave
action: measurements of an important ecological parameter
on rocky shores on Anglesey. Jour. Exp. Mar. Biol. Ecol.
2:46-63.

LINSENMEYER, T. A. 1975. The resistance of five species of
Polyplacophora to removal from natural and artificial sur-
faces. Veliger 18(Suppl.):83-86.

LUBCHENCO, J. & S. D. GAINEs. 1981. A unified approach to
marine plant-herbivore interactions. I. Populations and com-
munities. Ann. Rev. Ecol. Syst. 12:405-437.

LUBCHENCO, J. & B. A. MENGE. 1978. Community develop-
ment and persistence in a low rocky intertidal zone. Ecol.
Monogr. 59:67-94.

MENGE, B. A. 1976. Organization of the New England rocky
intertidal community: role of predation, competition, and
environmental heterogeneity. Ecol. Monogr. 46:355-393.

Meyer, G. R. & A. K. O’GoweER. 1963. The ecology of six
species of littoral gastropods. I. Association between species
and associations with wave action. Aust. Jour. Mar. Fresh-
water Res. 14:176-193.

MILLER, S. L. 1974. Adaptive design of locomotion and foot
form in prosobranch gastropods. Jour. Exp. Mar. Biol. Ecol.
14:99-156.

OTAiIza, R. D. & B. SANTELICES. 1985. Vertical distribution

Page 357

of chitons (Mollusca: Polyplacophora) in the rocky intertidal
zone of central Chile. Jour. Exp. Mar. Biol. Ecol. 86:229-
240.

PAINE, R. T. 1966. Food web complexity and species diversity.
Amer. Natur. 100:65-75.

PAINE, R. T. 1976a. Size-limited predation: an observational
and experimental approach with the Myzilus-Pisaster inter-
action. Ecology 57:858-873.

PaINE, R. T. 1976b. Biological observations on a subtidal Myt-
ilus californianus bed. Veliger 19:125-130.

PAINE, R. T. 1980. The third Tansley lecture. Food webs:
linkage, interaction strength and community infrastructure.
Jour. Anim. Ecol. 49:667-685.

PaINE, R. T. & S. A. LEvIN. 1981. Intertidal landscapes: dis-
turbance and the dynamics of pattern. Ecol. Monogr. 51:
145-178.

PAINE, R. T. & R. L. Vapas. 1969. Calorific values of benthic
marine algae and their postulated relation to invertebrate
food preference. Mar. Biol. 4:79-86.

PEARSE, J. S. 1978. Reproductive periodicities of Indo-Pacific
invertebrates in the Gulf of Suez. III. The chitons Acantho-
pleura haddoni Winckworth and Onithochiton lyelli (Sower-
by), and the abalone Haliotis pustulata Reeve. Bull. Mar.
Sci. 28:92-101.

RICKETTS, E. F., J. CALVIN & J. W. HEDGPETH (revised by D.
W. PHILLIPS). 1985. Between Pacific tides. 5th ed. Stanford
Univ. Press: Stanford, California. 652 pp.

SAKKER, E.R. 1986. Seasonal reproductive cycles of three Aus-
tralian species of chitons (Mollusca: Polyplacophora). Int.
Jour. Invert. Repro. Devel. 10:1-16.

SOUTHWARD, A. J. 1953. The ecology of some rocky shores in
the south of the Isle of Man. Proc. Trans. Liverpool Biol.
Soc. 59:1-50.

SOUTHWARD, A. J. & J. H. ORTON. 1954. The effects of wave
action on the distribution and numbers of the commoner
plants and animals living on the Plymouth breakwater. Jour.
Mar. Biol. Assoc. U.K. 33:1-19.

STEPHENSON, T. A. & A. STEPHENSON. 1972. Life between
tidemarks on rocky shores. W. H. Freeman & Co.: San
Francisco. 425 pp.

The Veliger 30(4):358-368 (April 1, 1988)

THE VELIGER
© CMS, Inc., 1988

Observations on the Larval and Post-Metamorphic Life of

Concholepas concholepas (Bruguiére, 1789) in

Laboratory Culture

by

LOUIS H. DiSALVO

Department of Aquaculture, Universidad del Norte, Casilla 480, Coquimbo, Chile

Abstract.

Observations were made in the laboratory on the postcapsular life of the Chilean “loco,”

Concholepas concholepas. Spontaneously eclosed veligers were cultured on two separate occasions, initiated
in October 1984 and in July 1985. Veligers fed on monospecific cultures of microalgae grew from an
initial shell length of 250 wm to near 1700 um during periods of 111 to 124 days. Of several tens of
thousands of early larvae, only seven individuals could be brought through metamorphosis, of which
only one survived and was cultured to juvenile size. About 60 competent veligers were captured at sea
with a neuston net, and returned to the laboratory where about 50% passed metamorphosis. Of these,
11 were cultured to 10-20 mm during a 3-mo period.

Aspects of the external morphology, growth, and behavior of larvae and postlarvae are reported for
the first time for this species. The larvae produce a four-lobed velum and employ a byssal thread for
flotation. They produce a distinctive lip on the larval shell indicating readiness for metamorphosis. The
propodium functions actively in adherence to substrates at metamorphosis, making this species highly

adapted for recruitment in the wave-swept Chilean intertidal zone.

INTRODUCTION

Concholepas concholepas (Bruguiére, 1789), an unusual
muricid gastropod of the South American temperate west
coast, is both biologically interesting and of high commer-
cial value. It is the last surviving species of a genus whose
other six members became extinct before or during the
Pleistocene (STUARDO, 1979). The existing species, com-
monly referred to in Chile as the “loco,” occurs from the
intertidal zone to depths of 40 m, and has a geographical
range from the central coast of Peru to the southern tip of
Chile. Ecologically, locos are first-level carnivores that prey
upon filter feeders such as the barnacles, mussels, and
tunicates abundant on the rocky Chilean coast (CASTILLA
et al., 1979). Locos reproduce by depositing egg capsules
on subtidal rocks, primarily during the winter months.
After an incubatory period of one or two months, veliger
larvae hatch from the capsules and enter the coastal plank-
ton for periods estimated to be about three months, after
which the later veligers settle in the high intertidal zone
during the spring and summer months (CASTILLA, 1982).

Concholepas concholepas represents the largest gastropod
fishery in the world (FAO, 1981). Fueled by a strong
export demand beginning in the 1970s, landings of this

species reached 24,858 metric tons (MT) by 1980 (CastTI-
LLA & JEREZ, 1986). By 1984 the total catch had dropped
to 11,100 MT (“SERNAP, 1985) with declines in catch
per unit effort demonstrated on a localized basis (GEAGHAN
& CASTILLA, 1986). The author participated on an advi-
sory panel in 1986 and 1987 convened by the Chilean
national fisheries service (SERNAP) in order to help plan
regulations designed to avoid overexploitation of the loco
fishery. Among the panel’s recommendations has been the
need to study the planktonic and early recruitment phase
of the loco life cycle, and the feasibility of its mass pro-
duction under artificial conditions. Although numerous
studies have been made on diverse aspects of the biology
of the loco (see review in CASTILLA, 1982) it had not, until
the present study, been cultivated in the laboratory.

The present study investigated aspects of the larval and
postlarval biology of Concholepas concholepas, and used
some elements of our bivalve hatchery facilities to examine
the feasibility of its mass culture. The first successful lab-
oratory culture of the species is now reported, with ob-
servations on its external morphology and behavior through
the planktotrophic phase and metamorphosis. The behav-
ior of loco veligers in laboratory aquaria led us to sample

L. H. DiSalvo, 1988

for wild specimens in coastal surface waters. Success in
this endeavor included the first recovery of advanced veliger
larvae, followed by their metamorphosis and growth in the
laboratory; these results lent critical support to the oth-
erwise limited success of larval culture in the laboratory.

MATERIALS anD METHODS

Attempts at culture of postcapsular veligers of Concholepas
concholepas were initiated in months when mature egg
capsules became available in the local habitat. The first
culture was initiated in October 1984 and the second in
July 1985. Capsules were collected by a diver at 3-5 m,
from the surfaces of subtidal rocks near the mouth of
Herradura Bay (30°S); capsules containing mature larvae
were chocolate brown in color. Capsules were maintained
in unfiltered, aerated seawater, which was changed daily,
at ambient temperatures near 16°C until hatching was
observed. As these cultures involved trial and error in
handling the larvae, we describe only the methods from
the second culture which was more successful.

About 10° actively swimming veligers were collected on
a 100-um aperture nylon screen (Nytex Co.) within 16 h
of their emergence from the capsules. The larvae were
washed with 1-uwm filtered, UV treated seawater, and dis-
tributed evenly by visual estimate into 10 10-L plastic
pails. The water was renewed every other day. To avoid
breakage of the fragile larval shells, the larvae were always
caught on the 100-um screen without removing it from the
water (D’Asaro, 1965). Culture water was treated with
25 mg/L chloramphenicol (Merck Co.) during the first
10 water changes in an attempt to eliminate bacterial in-
fections that might have been acquired within the capsule.
After the early water changes, antibiotic treatment was
administered as needed when microscopic examination
showed incipient bacterial infections of the larvae.

A number of empirical trials were made with early
larvae to determine acceptable temperature, food, and lar-
val density; larval survival, growth, and behavior were used
to evaluate the success of these trials. Larvae were offered
monospecific cultures of microalgae that were available
from our bivalve hatchery production system. These in-
cluded Tetraselmis sp., Pavlova sp., Chaetoceros sp., Iso-
chrysis galbana (Tahitian strain), and a Pseudoisochrysis sp.
Advanced larvae were given small amounts of mixed algae
of the above species in an attempt to vary the nutritive
sources in addition to the daily monospecific food ration
found to be best for early larvae.

Shell fouling of the larvae by bacteria and stalked pro-
tozoa sometimes mechanically interfered with larval swim-
ming and contributed to a deterioration in water quality.
Also, free-living protozoa and copepods occasionally ap-
peared as contaminants in the cultures. These problems
were treated by administering 1-min tap-water rinses to
the larvae at the time of water change, usually eliminating
the contaminants without observable effects on the larvae.

Larvae were routinely observed in a 25-mL plankton

Page 359

chamber using an inverted microscope, and were measured
with a calibrated ocular micrometer. Shell length in this
report refers to the major length from the tip of the siphonal
canal to the apex of the shell as seen in silhouette. After
metamorphosis, shell length was measured using the ocular
micrometer in a stereo microscope, and later with a ruler,
estimating to the nearest 0.5 mm. Calipers were not used
owing to the risk of breaking the fragile shells. Some ob-
servations of shells and radulae were made using a JEOL
Corp. model JSM T300 scanning electron microscope
(SEM).

The single laboratory cultured postlarva that survived
past metamorphosis in November 1985 was maintained in
an aerated culture pail with daily changes of ambient
seawater at room temperature of about 16-18°C. Initially
the specimen was kept on a scallop shell that was collected
from the local intertidal zone and was lightly fouled with
microbial slime films, small polychaetes, barnacles, and
bryozoans. At about 8 mm in length, it was transferred to
a similarly encrusted stone collected from the low intertidal
zone in the bay, upon which had been found a naturally
recruited loco of about the same size. At about 12 mm in
length, juveniles of Semzmytilus algosus (Gould) were added
to the system as prey.

Recovery of naturally occurring larvae from plankton
was accomplished by towing a buoyed-frame neuston net,
2 m in length, with 600-um mesh openings. The mouth
of the net was rectangular, measuring 40 cm high by 80
cm wide, and was floated to sample the top 20 cm of the
sea surface. One-kilometer hauls were made between De-
cember 1986 and March 1987, in and around the mouth
of Herradura Bay. Loco veligers were recognized by their
similarity to laboratory reared larvae, and were easily sep-
arated from other plankton by their tendency to fall to the
bottoms of the collecting vessels and adhere firmly in place.
Larvae were handled with a small camel’s hair brush to
avoid breaking their shells. Veligers so collected were in-
troduced into a laboratory aquarium containing naturally
encrusted stones from the intertidal zone and a constant
flow of ambient seawater. The effluent pipe was screened
with 1-mm mesh so as not to lose swimming veligers. ‘These
larvae were observed daily for evidence of metamorphosis
and those passing metamorphosis were transferred to a
rearing system where they were observed and measured
periodically. Natural substrates used in setting and rearing
were lightly populated by microbial slime films, crustose
red, green, and brown algae, as well as by small barnacles,
bryozoans, polychaetes, and sponges. Large invertebrates
were eliminated, leaving some clean surfaces on the stones.
Juveniles of Semimytilus algosus were added to the system
as prey.

RESULTS

Of the many thousands of larvae placed in culture during
two successive years, few larvae survived the experimental
period to pass metamorphosis. ‘Two larvae from the 1984

Page 360

culture and five larvae from the 1985 culture passed meta-
morphosis; all other larvae died during the course of the
cultures. Figure 1 plots the sizes of the largest larvae pro-
duced in the cultures over time periods lasting from 111
to 124 days. Of the five postlarvae produced in the 1985
culture, only one survived more than a few days and was
raised to a size in excess of 20 mm (Figure 6).

Sources of Mortality

The veligers suffered chronic mortality punctuated by
irregular mass mortalities at all stages of their develop-
ment. Microbial diseases often appeared in the cultures,
with at least four types of infection clearly definable. The
first of these was internal necrosis of early larvae by a
purple-pigmented microorganism that we believe, based
on unpublished data, to be a bacterium contracted during
the capsular developmental phase. A second type of infec-
tion was produced by a finely filamentous microorganism,
extensively investing the mantle edge of the larvae, causing
debilitation and death. Larvae infected in this manner
failed to respond to antibiotic treatment, suggesting that
the infection was fungal. A third type of infection included
a green-pigmented microorganism that infected the basal
region of the compound velar cilia, causing piecemeal loss
of ciliary tufts. This infection could be arrested by the
addition of chloramphenicol to the culture water; most
larvae infected in this manner recuperated and regenerated
the lost cilia. A fourth problem was attack of the larvae
by a ciliate protozoan (7etrahymena sp.), an occasional
parasite that is capable of invading the larval digestive
gland causing death of the host. This disease may be the
primary cause of chronic mortality in cultures of Concho-
lepas concholepas at all stages, and has also been the cause
of mass mortalities of scallop postlarvae in our hatchery
(unpublished data). No effective control measures have
been found for this disease in the loco cultures. Other losses
of larvae may be due to shell breakage during handling,
although larvae do have limited capacity to repair damage
to the leading shell edge and siphonal canal.

The following is a sequential account of events observed
in our cultures, based on observation of the largest larvae
recoverable at each time.

Early Larvae

Eclosion from capsules occurred slowly over several days.
Most larvae swim actively in the water column, rising to
the surface in ambient light directed from above. Some
larvae, perhaps those not fully developed, settle to the
bottoms of the eclosion pails. At this stage the protoconch
measures 240-260 um, and is semitransparent with tu-
berculate ornamentation (Figure 2A). The velum consists
of two round lobes, each about 150 um in diameter (Figure
2B). The head region between the velar lobes has eyespots
on either side of the mouth (Figure 2C) and one short
cephalic tentacle that is anteroventral to the right eyespot

The Veliger, Vol. 30, No. 4

and has four apical sensory bristles. A pair of statocysts
is visible posterior to the eyespots. At hatching the foot
does not extend beyond the posterior border of the pro-
toconch, is immobile, and has a few short sensory bristles
at its posterior extremity. At hatching the larval gut retains
a small amount of vitelline material which is utilized in a
few days. Larvae begin feeding in 24-48 h, as evidenced
by the appearance of microalgal food in the digestive tract.
If food is withheld after the larvae begin feeding, die-off
begins after 3 days with complete mortality after 7 days.
Larval kidneys emerge from the mantle cavity and are lost
at about 24 h after hatching. Shell growth begins soon
after the initiation of feeding, appearing as successive in-
crements on the protoconch.

Among the five species of microalgae offered to replicate
samples of larvae in several trials throughout the culture
period, /sochrysis galbana (Tahitian strain) was the most
acceptable, as evidenced by digestion of the algal cells and
the survival and growth of the larvae. Excessive numbers
of microalgae in the water induce the veligers to produce
mucus, which comes away from the larvae in thin, algal-
laden strands. This material settles, producing undesirable
organic contamination in the culture vessels. Acceptable
initial culture conditions include one larva and about 2 Xx
10° microalgal cells per mL of culture water. As the larvae
grow, the food ration is increased according to the larval
capacity to ingest the algae without producing mucus
strands.

The veligers appear to be positively phototactic through-
out the entire culture period. When placed in cylindrical
plankton chambers for observation with an inverted mi-
croscope they swim upward toward the light source and
drop quickly to the bottom when the light is extinguished.

One to Three Weeks

By the end of the first week, a dorsocentral beak begins
to form on the shell over the cephalic region and the si-
phonal canal develops on the left side of the shell. After
about 10 days the shell begins to darken, and by three
weeks it is dark amber-brown in color. Shell color is due
to a periostracum that can be dissolved away with 0.1 N
NaOH. At 10 days, black chromatophores are scattered
over the dorsal surface of the foot, and the foot begins to
show its first weak contractions. A few sensory bristles
appear around the margin of the foot.

At about three weeks, a mantle tentacle appears inside
the right mantle cavity, barely visible inside the shell edge.
The velum has doubled its original size, and begins to
show lateral indentations. The outer margin of the velum
develops brown pigmentation demarcating the line of or-
igin of the locomotory (compound) cilia.

Four to Seven Weeks

By four weeks the largest larvae have completed the first
shell revolution around the protoconch, and measure about

L. H. DiSalvo, 1988

Shell Length, mm

04 (40,000) (10000)

03 ©

Page 361

© Ox /
ttx P
1
ae Xx
eat
A 23
A
z&

(1200) (400) (10) (1)

10 20 30 40 50 60

80 90 100 110 120 130

TIME, days

Figure 1

Sizes of largest individual veligers of Concholepas concholepas occurring in cultures initiated in October 1984 (circles)
and July 1985 (triangles). Dorsal silhouette views of larvae show relative sizes of the larvae with time and
development of the velum. Numbers in parentheses indicate approximate number of larvae surviving with time
during the 1985 culture. Key: arrows, day of metamorphosis and number of specimens passing metamorphosis; X,
death of a metamorphosed specimen; P, postlarval growth of single survivor, also plotted in Figure 6.

650 wm. The beak, with its central beak line, and the
siphonal canal become prominent shell features (Figure
3). The shell becomes ornamented with radial lines (now
coalescing from what began as lines of tubercles). The
radial lines may act as reinforcement for the otherwise
fragile shell. The velum has begun to elongate into four
lobes, giving the veliger a “butterfly” appearance (Figure
3B). The velum remains unpigmented except for the outer
margin. The single cephalic tentacle has begun to elongate
and develop numerous sensory bristles.

The veligers swim freely in the culture pails at this

stage, with no definable behavior pattern evident. The
massing of larvae on the bottoms of the pails is often,
although not always, a sign of developing disease or nu-
tritional problems for a given group of larvae.

A notable development in the life of this veliger occurs
beginning at 3-4 weeks with the appearance of a byssal
thread issuing ventrally from a small gland at the extreme
tip of the foot (Figure 3B). The byssal thread is about 1
um in thickness and may extend for several centimetres.
Larvae become capable of using the byssal thread for flo-
tation, and are sometimes observed suspended in undis-

Page 362

Figures 2A, B

External aspects of newly eclosed veliger larvae of Concholepas
concholepas, shell length 260 um. A. Right lateral view (shell
only): u, umbilicus at center. B. Dorsal view: rt, right cephalic
tentacle; lc, locomotory cilia.

turbed culture water with the thread adhering to the water
surface film. These larvae could be gathered by inserting
a dissecting needle through the air-water interface and
catching the threads; threads were strong enough that in-
dividuals could be lifted from the water. Thread production
could be induced in freely swimming larvae by short vig-
orous agitation of the culture water.

At about 40 days, the primordium of the second cephalic
tentacle appears on the left side of the head region. The
shell measures about 800 um and has a pronounced beak.
The four velar lobes become horizontally elongate and can
measure a total width of 1350 wm when extended. The
chromatophores on the foot become more numerous and
diffuse, producing dark gray coloration; the foot increases
its contractile movements. The propodial mucus gland ap-

The Veliger, Vol. 30, No. 4

Figure 2C

Anterior view (locomotory cilia excluded): e, eyespot; st, statocyst;
rt, right cephalic tentacle; vl, velar lobe; m, larval mouth.

pears as a horizontal slit across the anterior of the pro-
podium, a structure that is now beginning to elongate and
show independent movement. The secretion of a purple
dye, typical of adult locos, is first observed at about 50
days as pigment granules deposited on the dorsum of the
larval operculum.

Replicate cultures run between day 20 and 50 under
the same conditions except for larval densities, showed
significantly (P = 0.95) better growth of the larvae when
maintained at densities of 250/L when compared with
those at densities of 500 or 1000 larvae/L. Maximum shell
length attained in these tests was 770 wm with 250 lar-
vae/L, 624 um with 500 larvae/L, and 562 um with 1000
larvae/L. Individuals from a replicate culture with 250
larvae/L kept at 13-14°C were significantly (P = 0.95)
smaller than those of the other groups maintained at 16-
18°C; the maximum size recorded for this group was 580
um. Unlike the other cultures, the cooler replicate expe-
rienced almost complete mortality near the end of the test
period. Overall, larval densities had to be markedly de-
creased as the larvae grew in size, as they increasingly
showed a tendency to become entangled with byssal threads
or mucus strands. Nearing metamorphosis, the larval den-
sity had to be kept to 5-10 larvae/L.

Eight Weeks

The shell length measures 950-1000 um, with about 20
pm added daily to the leading shell edge. The beak and
siphonal canal continue to be prominent features of the
shell. Larvae are capable of crawling on the foot for periods
of up to 1 min during observations with the inverted mi-
croscope.

At 65 days, the extended foot measures about 950 wm,
of which the propodium occupies about 200 um. The pro-
podium is about 200 wm in breadth when extended, and
becomes active in dislodging mucus and algal debris from
the velum and shell margin.

L. H. DiSalvo, 1988

Page 363

Sambi

Ui

Figure 3

External aspects of one-month-old veliger larvae of Concholepas concholepas, shell length 650 wm. A. Right lateral
view (shell only): b, beak; bl, beak line (crest). B. Dorsal view: bg, byssal gland; bt, byssal thread; f, foot; s, siphonal

canal; rt, right cephalic tentacle; p, pigment.

Ten Weeks

Advanced larvae measure 1000-1200 um in shell length,
with a total velar extension of about 3200 um. The right
cephalic tentacle now measures about 260 um in length,
the left tentacle is about two-thirds this length, and the
eyes are now located in the tentacle bases. The head and
foot are now black, but the mantle edge, tentacle tips, and
velum show little or no pigmentation. Veligers are capable
of crawling on the foot for 3 min before they fall over. The
operculum saddles the foot, is about 400 um wide, and is
stained purple.

At this stage larvae rarely swim, and are typically seen
hanging by their byssal threads equidistant from one another
in the culture water. The velum remains open and actively
filtering. If released from the byssal threads, larvae drop
to the bottom of the pail, but soon rise again in the water
column. If they encounter the walls of the pail, they “push
off” with a clapping motion of the velar lobes.

Twelve Weeks

The left tentacle reaches about three-quarters the length
of the right tentacle. Shell growth has slowed, with largest
veligers measuring 1400 um (Figure 4). The gaps on either
side of the beak have filled with shell, and the remnant of
the beak is only a small projection.

Fourteen Weeks

Between 90 and 110 days, shell growth stops after com-
pleting 2.5 revolutions around the protoconch. Although
early observations had suggested that ornamentation lines
reflected daily growth increments, these “daily growth lines”
could not be correlated with the known number of days
in culture of the larvae. Using the SEM, what appeared
to be true daily growth increments were demarcated by
fine sutures in the shell. The cephalic tentacles are ap-
proximately equal in length, although the left tentacle
tends to remain shorter than the right. The eyes project
dorsolaterally near the base of each tentacle. A conical
mentum, indicative of the site of the future opening of the
postlarval mouth, is evident between the tentacles (Figure
4B).

The major event at this stage, indicating the termination
of larval shell growth, was the production of an upturned
lip around the leading edge of the shell (Figure 5). On
two successive days metamorphosis was observed 24 h after
the formation of the lip in each of two larvae from the
culture initiated in October 1984 (Figure 1). Other lipped
larvae from culture, as well as comparable larvae captured
at sea, failed to undergo metamorphosis for days or weeks
without further growth of the shell when maintained in
clean culture vessels with microalgal food.

Page 364

pad ee
Ge aye !

aA

Ss
AWW

y

Figure 4

External aspects of three-month-old veliger larvae of Concholepas
concholepas, shell length 1400 um. A. Anterodorsal view: rt, right
cephalic tentacle; s, siphon; ol, ornamentation lines; f, foot; bt,
byssal thread. B. Anterior view of cephalic region (locomotory
cilia omitted): SH, shell; s, siphon; me, mantle edge; e, eye; vl,
velar lobe; rt, right cephalic tentacle; mt, mentum; m, larval
mouth; po, post oral ciliary band; fg, food groove; pmg, propodial
mucus gland; p, propodium; op, operculum.

The lipped shells of seven larvae from culture that passed
metamorphosis measured between 1350 and 1690 um in
shell length, with velar extensions of up to 6500 um. Thir-
ty-one lipped larvae captured at sea measured between
1590 and 1830 wm (« = 1686; SD = 77).

The Veliger, Vol. 30, No. 4

Postlarval Concholepas concholepas prior to appearance of teleo-
conch, shell length 1690 um: pml, premetamorphic lip; e, eye; f,
foot.

Behavior Related to Settling and Metamorphosis

Development of a new behavior pattern becomes ap-
parent after lip formation on the shell, preceding meta-
morphosis. The veliger acquires the capability of quick
attachment to surfaces with which it comes in contact by
the use of the suckerlike action of the (cupped) propodium.
This behavior was first noted when attempting a routine
transfer of lipped larvae with a glass pipette, to which they
stuck immediately and with great tenacity.

At the lipped stage, veligers are capable of continuous
crawling; we observed two of these veligers to settle on a
natural substrate over which they crawled for periods of
24 h, after which they returned to a swimming existence.
One veliger, accidentally left emersed for 8 h, returned to
its swimming existence when returned to the water, and
later passed metamorphosis. A further behavioral adap-
tation observed in lipped larvae may be referred to as
“bubble capture.” When strongly agitated by a jet of sea-
water from a hose, each veliger was observed to capture
an air bubble using the foot, thus permitting it to float
after loss of the byssal thread, and with the velum retracted.
When left in calm water, each veliger released its bubble
and resumed normal activity. This behavior was repeatedly
elicited with dozens of larvae on different days.

Metamorphosis and Early Growth

Detailed observations of metamorphosis could not be
made owing to the few larvae available and the unpre-
dictability of the onset of metamorphosis. Of the total of
seven larvae from the two laboratory cultures that passed
metamorphosis, three died owing to accidents in handling,
three failed to accept food and died without further growth
in 3 to 7 days, and one survived and grew to juvenile size.
The surviving postlarva was cryptic and difficult to find

L. H. DiSalvo, 1988

mm

Length

Shell

Page 365

1. 0 GQ “QW Ge ZOMMNNCOMmN TS ONL CON Nn1IO NNT 20
TIME (days
Figure 6

Growth after metamorphosis in the laboratory of 11 locos captured at sea as pre-metamorphic veligers (dots) + 1
SD (L, = 1.16 + 0.143¢; r = 0.98). The growth of the single loco that survived through metamorphosis in laboratory
culture is shown by the dotted line. m, sizes of specimens at metamorphosis.

while on its natural substrate. The first deposition of te-
leoconch material was observed at about 24 h post-meta-
morphosis as an extension of the siphonal canal. At about
48 h, the teleoconch became visible as a white ring around
the shell margin. ‘Teleoconch material deposited in the first
few days was unpigmented, deposited in marked daily
increments, and showed rugosity typical of advanced shells
of Concholepas concholepas. A trunklike proboscis devel-
oped within 48 h of metamorphosis. This specimen grew
to a size of 13.5 mm in the first four months post-meta-

morphosis (Figure 6). The first invertebrate prey taken by
this specimen is unknown, although the specimen rasped
the substrate at a very early stage, and later grazed on
microalgae from the walls of the culture pail. Even after
it began active predation on Semimytilus algosus 1t contin-
ued to graze clean 1-2 cm circular areas in a film of diatoms
and bluegreen algae that had accumulated on the walls of
the pail.

About 60 lipped larvae were captured at sea, half of
which passed metamorphosis in the laboratory; 11 of these

Page 366

survived the postlarval phase and were cultured to larger
sizes (Figure 6). These veligers passed metamorphosis spo-
radically, rather than en masse, over periods of several days
after their capture. Subsamples of this group failed to pass
metamorphosis over a 48-h period when held in clean
culture pails with aeration. Crawling veligers and postlar-
vae became negatively phototactic and were observed with
difficulty on natural substrates owing to their small size,
cryptic habits, and dark coloration. Remarkably, in a few
days after metamorphosis, most of the black pigmentation
disappeared from the head and foot, which assumed a
whitish translucent color. Gray pigmentation was slowly
regained by these structures, beginning about two months
after metamorphosis.

Of all the crawling veligers observed, none was observed
to possess a partially resorbed velum, suggesting that the
loss of the velum is abrupt, possibly by swallowing (FRET-
TER, 1967). Newly metamorphosed postlarvae are found
on the cleanest available parts of the substrate, including
unpopulated surfaces, barnacle shells, and calcareous al-
gae. They possess a well-developed radula at metamor-
phosis, of which the rachidian teeth have a morphology
distinct from those of adult Concholepas concholepas (Fig-
ure 7). Postlarvae rasp microbial films from both culture
pails and natural substrates, leaving cleaned areas of sev-
eral square millimetres daily. The digestive tract of a sac-
rificed 3-mm long postlarva reared on a natural substrate
contained great numbers of bacteria, as well as some dia-
toms and a few fragments of fleshy encrusting red and
brown algae.

The 11 specimens maintained in culture grew to 11-19
mm in length during the first 90 days, with a mean growth
rate of 0.143 mm/day (Figure 6). They remained on a
home range of about 10 x 20 cm on the underside of a
stone during the day, and foraged over the whole stone at
night. Upon reaching a few millimetres in size they began
to perforate, paralyze, and consume animal prey.

DISCUSSION

The rearing of long-lived planktotrophic veliger larvae
poses serious technical problems, as mentioned by D’ASARO
(1965) in his study of Strombus gigas. Although there were
similarities between the present study and that of D’Asaro,
the rearing of Concholepas concholepas was even more prob-
lematical owing to the unusual longevity of these larvae.
Personal communication with workers developing com-
mercial cultures of S. gigas under proprietary conditions
has suggested that the time to maturity of these larvae
became progressively reduced as optimal feeding and han-
dling methods were discovered. Similar advances may be
expected in the culture of locos. The high levels of mortality
in our cultures were disturbing, and reflect the present
lack of knowledge concerning nutritional and environ-
mental requirements of loco veligers. These larvae may
indeed change food requirements as they grow and develop
new organ systems (D’AsaARO, 1965). Disease problems

The Veliger, Vol. 30, No. 4

may be no more than a response to stress imposed by
presently suboptimal culture conditions.

In the past, Castilla and co-workers (unpublished data)
recovered molluscan larvae in vertical plankton hauls not
far from our laboratory, but were unable to confirm the
presence of advanced loco larvae in their samples owing
to the unavailability of authentic reference specimens. Our
experience with larvae in laboratory cultures allows the
immediate recognition of loco larvae captured at sea. Our
repeated collection of advanced veliger larvae in the surface
plankton confirms observations made in the laboratory that
these larvae tend to rise to the surface of the water column.
On days when we captured naturally occurring loco larvae
at the sea surface, hauls made with the same net towed at
2-m depth over the same transect captured none of these
larvae. Metamorphosis and growth of field-captured larvae
in the laboratory duplicated in a few days a result that
had taken months to achieve by way of the time-consuming
laboratory cultures.

Larval Strategies

The present laboratory and field observations suggest
some of the evolved mechanisms whereby Concholepas con-
cholepas has survived and become widely distributed, and
permits hypothetical reconstruction of the natural history
of the larval phase of the life cycle. Larvae may require
up to four months to reach the lipped form, ready for
metamorphosis. Lipped larvae may survive for many more
weeks, suspended by the byssal thread and feeding while
drifting in oceanic currents in a manner similar to that
described by SIGURDSSON et al. (1976) for plantigrade bi-
valve larvae. (KENSLEY [1985] discovered a relict fossil
population of locos in southwest Africa which he attributed
to the possible long distance dispersal of larvae by the West
Wind Drift.) Larvae may maintain themselves near the
water surface by velar swimming governed by their positive
phototaxis. They may thus be maintained near the coast-
line by surface circulation driven by prevailing onshore
winds active during the daytime. Byssal threads inserted
in the air-sea interface may tow larvae along the surface
when acted upon by these winds. Upon arrival at the shore,
larvae tossed by the surf may effect “bubble capture,”
maintaining themselves in the neuston to be carried ashore
with the surface slick or in sea foam. Upon being cast
ashore, larvae quickly settle on the rocks using the pro-
podium, seek a protected spatial niche, metamorphose, and
begin feeding on microbial films. They become cryptic
inhabitants of the rocky shore infauna until they have
produced a resistant shell and can begin active feeding on
invertebrates.

All 60 larvae caught by us at sea during a two-month
period were competent for metamorphosis (lipped). These
may have been the last individuals representing the re-
productive cohort hatched during 1986, assuming that the
majority of larvae of that year class had recruited to the
plankton by August (CASTILLA, 1982). The early growth

L. H. DiSalvo, 1988

of postlarval locos (Figure 6) appears to be linear during
the first few months of life, and may be continuous with
the growth curve obtained by GUISADO & CASTILLA (1983)
for naturally occurring populations ranging in size from
11 to 57 mm. We do not know what factors induce meta-
morphosis in loco veligers, although chemosensory rec-
ognition of suitable substrates probably plays an important
role (MorsE ef al., 1980).

Observation of algal feeding by juvenile locos is not
inconsistent with known omnivorous feeding patterns ob-
served in life histories of other juvenile muricids (M. R.
Carriker, personal communication), but it is remarkable
that algal feeding did not cease even after the young locos
had begun to feed actively on mussels. Also remarkable is
the finding that the radular teeth of the postlarva were
distinct from those of the adult (Figure 7).

Prospects for Mass Culture

The limited knowledge presently available from our
laboratory cultures of Concholepas concholepas suggests that
mass commercial culture of this species is infeasible in the
near future. Larval locos are simply not suitable for the
presently used techniques of tank culture. Possession of a
large, fragile, and efficient velum, as well as a highly
specific mechanism for flotation (byssal thread), has adapt-
ed this species to a solitary drifting existence in oceanic
waters. A widely separated distribution at the sea surface
was demonstrated during our plankton hauls, where the
net had to be towed several kilometres to obtain a very
few larvae. On our most successful day in January 1986
we obtained a total of 47 larvae from seven separate 1-km
hauls. Implications of this mode of life for hatchery design
include maximization of culture volume per larva, contin-
uous feeding with dilute suspensions of microalgae, and
maintenance of high water quality for extended periods of
culture. If such conditions are not maintained, larvae be-
come entangled with byssal threads or mucus strands, fall
to the tank bottom, and are subject to microbial attack.

The above-mentioned hatchery requirements are un-
economical compared with methodology used in mass rear-
ing of bivalve larvae (DISALVO et al., 1984) or lecithotro-
phic gastropod larvae (OWEN et al., 1984), which can be
maintained at high densities and pass metamorphosis in a
few days or weeks. Mass culture of the loco might be based
on the capture of lipped veligers at sea, with transfer to
hatchery settling and rearing systems. Presently, such de-
velopment is limited by the lack of knowledge of season
and geographic location of larval concentrations off the
coastline.

Resource Management

If culture seems a distant possibility, then preservation
of the resource lies now in the correct management of
remaining natural stocks. Such management has been hin-
dered by logistical difficulties in the estimation of popu-

Page 367

Spm

——

50 ym
Figure 7

Rachidian teeth from a postlarval Concholepas concholepas. A,
from anterior teeth; A, from posterior teeth. Adult loco rachidian
tooth (B) presented for comparison of form.

lation parameters. The procedure of capturing pre-meta-
morphic larvae at sea provides a new method for the indirect
monitoring of the reproductive success of the remaining
stocks of locos. This technique can be made at least semi-
quantitative by the establishment of standard transects to
be monitored routinely throughout the year, and calcu-
lating the number of competent larvae per km? of sea
surface. Yearly counts of competent larvae near shore could
provide information on long-term trends in the reproduc-
tive success of the loco in the face of continued harvesting
pressure. The method proposed is unsophisticated and in-
expensive compared with diver surveys of loco populations
and with shoreside censuses of fishery success, which are
subject to many sources of bias. The measurement pro-
posed would not, however, predict actual recruitment to
the population, which should be measured by other means
and then correlated with larval counts.

ACKNOWLEDGMENTS

This research was sponsored by the Direccion de Inves-
tigaciones, Universidad del Norte, Antofagasta. | am grate-
ful for helpful correspondence from Dr. M. R. Carriker,
technical aid and suggestions from E. Martinez, E. Lara,
and E. Montes, and critical reading of the manuscript by
Dr. Matias Wolff. Drawings of loco larvae were executed
by Mr. Marco Leon, and I thank Mrs. Gilda Bellolio for

Page 368

meticulous dissection of the larval radula and operation of
the scanning electron microscope. Support for fieldwork
was provided by the Chilean Government Corporation for
the Promotion of Development (CORFO).

LITERATURE CITED

CASTILLA, J. C. 1982. Pesqueria de moluscos gastropodos en
Chile; Concholepas concholepas, un caso de estudio. Mono-
grafias Biologicas 2:199-212.

CAsTILLA, J. C., C. GuisaDo & J. CANCINO. 1979. Aspectos
ecologicos y conductuales relacionado con la alimentacion de
Concholepas concholepas (Mollusca: Gastropoda: Muricidae).
Biol. Pesq. 12:99-114.

CasTILLA, J. C. & J. JEREZ. 1986. Artisanal fishery and de-
velopment of a data base for managing the loco, Concholepas
concholepas, resource in Chile. Pp. 133-139. In: G. S. Jamie-
son & N. Bourne (eds.), North Pacific workshop on stock
assessment and management of invertebrates. Can. Spec.
Publ. Fish. Aquat. Sci. No. 92.

D’Asaro, C.N. 1965. Organogenesis, development, and meta-
morphosis in the queen conch, Strombus gigas, with notes on
breeding habits. Bull. Mar. Sci. Gulf Carib. 15:359-416.

DiSaA.vo, L. H., E. ALARCON, E. MARTINEZ & E. URIBE. 1984.
Progress in mass culture of Chlamys (Argopecten) purpurata
Lamarck (1819) with notes on its natural history. Revista
Chilena de Historia Natural 57:33-45.

F.A.O. (United Nations). 1981. Yearbook of fishery statistics.
Catches and landings. F.A.O., Fish. Ser.; Stat. Ser. No. 50.

FRETTER, V. 1967. The prosobranch veliger. Proc. Malacol.
Soc. Lond. 37:357-366.

The Veliger, Vol. 30, No. 4

GEAGHAN, J. & J. C. CAsTILLA. 1986. Use of catch and effort
data for parameter estimates for the loco (Concholepas con-
cholepas) fishery in central Chile. Pp. 168-174. In: G. S.
Jamieson & N. Bourne (eds.), North Pacific workshop on
stock assessment and management of invertebrates. Can. Spec.
Publ. Fish. Aquat. Sci. No. 92.

GuIsabo, C. & J. C. CAsTILLA. 1983. Aspects of the ecology
and growth of an intertidal juvenile population of Concho-
lepas concholepas (Mollusca: Gastropoda: Muricidae) at Las
Cruces, Chile. Mar. Biol. 78:99-103.

KENSLEY, B. 1985. The fossil occurrence in southern Africa of
the South American intertidal mollusc Concholepas concho-
lepas. Ann. 8. Afr. Mus. 97:1-7.

Morse, D. E., M. TEGNER, H. DUNCAN, N. HOOKER, G.
TREVELYAN & A. CAMERON. 1980. Induction of settling
and metamorphosis of planktonic molluscan (Haliotis) lar-
vae. III: signaling by metabolites of intact algae is dependent
on contact. Pp. 67-86. In: D. Muller-Schwarze & R. M.
Silverstein (eds.), Chemical signals. Plenum: New York.

OwEN, B., L. H. DiSALvo, E. EBERT & E. FONCK. 1984. Cul-
ture of the California red abalone Haliotis rufescens Swainson
(1822) in Chile. Veliger 27:101-105.

SERNAP. 1985. Anuario de estadistica en pesca 1984. Servicio
Nacional de Pesca. Santiago, Chile.

SIGURDSSON, J. B., C. W. TITMAN & P. A. Davigs. 1976. The
dispersal of young post-larval bivalve molluscs by byssus
threads. Nature 262:386-387.

STuaRDOo, J. 1979. Sobre la clasificacion, distribucion, y va-
riacion de Concholepas concholepas (Bruguiére, 1789): un
estudio de taxonomia beta. Biol. Pesq. 12:99-114.

NOTE ADDED IN PROOF

On 21 September 1987, 24 lipped veligers (< = 1780 um, SD = 100 wm) were captured in a surface
plankton haul about 2 km seaward of the mouth of Herradura Bay. These larvae were returned to the
laboratory setting system containing a natural substrate as described in the text, with a continuous flow
of seawater of 10 L/min at 15°C. This flow rate rate caused agitation within the system, and circulation
of the veligers over the substrate. Within 16 h (overnight) 22 of these veligers had passed metamorphosis,
settling both on the substrate and walls of the aquarium. This was taken as evidence that these larvae
could pass metamorphosis en masse in the presence of turbulent water.

The Veliger 30(4):369-371 (April 1, 1988)

THE VELIGER
© CMS, Inc., 1988

Spawning and Larval Development of the ‘Trochid
Gastropod Calliostoma ligatum (Gould, 1849)

ALAN R. HOLYOAK*

Department of Zoology, 574 WIDB, Brigham Young University, Provo, Utah 84602, U.S.A.

Abstract. Spawning and larval development through metamorphosis were observed in the trochid
gastropod Calliostoma ligatum. Gametes were broadcast into the water column, sperm in white puffs
and eggs in mucous strings. Larvae hatched as swimming veligers after 6 days, stayed in the water
column for 3 to 4 days, and metamorphosed after 12 days. Broadcast spawning and planktic larvae
indicate a more primitive reproductive strategy in C. /igatum than in other Calliostoma species which
attach to substrata eggs from which hatch metamorphosed snails.

INTRODUCTION

Reproduction in Calliostoma ligatum (Gould, 1849), a com-
mon and conspicuous member of intertidal and subtidal
communities along the Pacific coast of North America, has
not been studied in detail. Information concerning the re-
productive biology of this snail is limited to a brief report
by Hunt (1980) on the eggs and their release. Develop-
mental studies have been made on two other Calliostoma
species: C. zizyphinum (Linnaeus) (LEBOUR, 1936; CROFTS,
1955) and C. papillosum (Da Costa) (ROBERT, 1902).

This paper presents a description of spawning and de-
velopment through metamorphosis for Calliostoma ligatum
collected in the San Juan Islands, Washington, U.S.A., in
the winter and early spring of 1985. A comparison between
the development of C. ligatum and other Calliostoma species
is also made.

MATERIALS anp METHODS

Ten adults of Calliostoma ligatum were put in 800 mL of
filtered seawater and placed in direct sunlight. When the
water warmed, the snails began to release gametes.

Once spawning had commenced males and females were
segregated by sex, rinsed to remove gametes, and put into
800 mL of 10-15°C filtered seawater. Both sexes continued
to spawn after rinsing and transfer.

* Current address: Institute of Marine Sciences, University of
California, Santa Cruz, California 95064, U.S.A.

Eggs were pipetted from the bottom of the beaker and
from the water column as they were released, transferred
to 800 mL of fresh filtered seawater, and refrigerated until
sperm were collected.

Sperm (3-5 mL) were collected as they were ejaculated
and mixed with 100 mL of filtered seawater. This sperm
solution was used immediately to fertilize previously col-
lected eggs.

Approximately 100 eggs, or enough to nearly cover the
bottom of a beaker, were pipetted into 800 mL of filtered
seawater. Fertilization was accomplished by adding 2-3
mL of sperm solution to the eggs and gently agitating the
gamete mixture for a few minutes. Fertilized eggs were
rinsed to remove excess sperm. Beakers containing fertil-
ized eggs were placed in a running seawater table and
maintained at 7-9°C during development.

Cultures were periodically agitated, especially during
early developmental stages. ‘The water was changed each
2-3 h with freshly filtered seawater for the first day, and
daily thereafter. No food was given to hatched larvae.

RESULTS

Spawning was first observed on 23 February 1985 with
subsequent spawnings occurring through mid-April (Ta-
ble 1). Spawning occurred during all lunar phases and
included late morning and early evening hours. During
all spawns the water temperature was at least 10°C.

Snails of both sexes moved to the air-water interface
before releasing gametes.

Sperm were released as a milky white substance. No

Page 370

Table 1

Date, time of day, water temperature, and lunar phase
during five spawnings of Calliostoma ligatum.

Water

Date temp.

(1985) Time (°C) Lunar phase
23 Feb. 1700 10 New-1st Quarter
27 Feb. 1139 16 1st Quarter

1 Mar. 1815 11 1st Quarter—Full

9 Mar. 1915 10 Full
13 Apr. 1544 15 Last Quarter

size measurements of sperm were obtained. Cursory ob-
servations confirmed, however, that sperm were released
individually and not in packets and that they were very
active. Sperm release lasted 10-45 min.

Eggs were sheathed in mucous strands as they were
spawned. These strands were 1-3 mm wide, held 1-4 eggs
across the strand, and contained 10-90 eggs. Many pulses
of eggs were released per spawn. Female spawns lasted
39-60 min and individual females released more than 1500
eggs. Eggs were not secured to any surface by adults but
drifted to the bottom. The light green, granular eggs were
opaque and 225 um in diameter. The egg was separated
from a gelatinous coat by a 20-wm wide space. The ge-
latinous coat was 30 wm in width and a frilly chorion 215
um wide bordered that coat. An egg with its associated
structures had a diameter of 750 wm (Figure 1A).

Fertilization and Development

Upon sperm penetration, the space between the egg and
surrounding gelatinous coat increased from 20 to 50 wm
and the gelatinous coat increased from 30 to nearly 100
um in width (Figure 1B).

Development proceeded in a spiral cleavage pattern.
The first two cleavages were meridional, equal, and ho-
loblastic. The third cleavage was equatorial and unequal.
Subsequent cleavages and differential cell divisions re-
sulted in morula and then gastrula stages. For the timing
of development see Table 2.

Gastrulae produced cilia at one end and ciliary beating
caused spinning and rotation within the gelatinous coat.
These cilia later formed the prototroch of the trochophore
larvae (Figure 1C).

The shell gland and foot rudiment appeared during the
trochophore stage. Shell secretion soon followed with the
first sign of the larval shell being a shiny spot on one side
of the trochophore. On the opposite side of the larva, the
foot fold was becoming more prominent. Larvae soon
thereafter became veligers (Figure 1D).

As prehatched veligers, larvae continued to secrete shell
material and enlarge a now bilobate velum. The operculum
formed during this stage, the digestive gland was visible,

The Veliger, Vol. 30, No. 4

Figure 1

Developmental stages of Calliostoma ligatum. All scale bars rep-
resent 200 wm. A. Unfertilized egg: E, egg; GC, gelatinous coat;
CH, chorion. B. Fertilized egg: E, egg; GM, gelatinous coat
membrane. C. Trochophore: PTA, pretrochal area; PT, proto-
troch. D. Early veliger: V, velum; LS, larval shell; FF, foot fold;
FR, foot rudiment. E. Prehatching veliger with torsion nearly
completed: V, velum; F, foot; OP, operculum; DG, digestive
gland; LSP, larval shell pattern (which covers the entire shell);
SL, shell lip. F. Metamorphosed snail: AS, adult shell; MC,
mantle cavity; DG, digestive gland; LS, larval shell; OP, oper-
culum; F, foot; ET, epipodial tentacles; E, eyespot; CT, cephalic
tentacle.

and larval shells had a honeycomb pattern and a lip. Tor-
sion was also accomplished before hatching. At hatching
the larval shell had 1% whorls (Figure 1E).

Calliostoma ligatum hatched as a swimming veliger after
6 days and spent 3-4 days in the water column. Individuals
then went to the bottom where they spent 3-4 days crawl-
ing and swimming before metamorphosis occurred. During
this swimming-crawling stage epipodial tentacles formed
and the foot became mottled. At metamorphosis the velum
was sloughed off, cephalic tentacles and eyes became readi-

A. R. Holyoak, 1988

Page 371

Table 2

Timetable of the development of Calhiostoma ligatum. Times
are mean values for five cultures at 7-9°C.

Time Stage

Oh Fertilization

SH oh Ist cleavage

5.8 h 2nd cleavage

7.4h 3rd cleavage

1.8 day Ciliated gastrula
2.1 day Trochophore

2.4 day Shell visible

2.6 day Foot fold visible

3.1 day Veliger

3.5 day Shell pattern visible
4-5.5 day Torsion

6 day Hatching

9.5 day Swimming-crawling
12.2 day Metamorphosis

ly visible, and secretion of the adult shell was begun (Fig-
ure 1F).

Approximately 90% of fertilized eggs reached meta-
morphosis.

DISCUSSION

Spawning in Calliostoma ligatum depends on neither lunar
phase nor on time of day since spawning occurred during
all lunar phases and times of day as shown in Table 1.
Elevated water temperature appears to be a primary factor
in inducing spawning.

When Calliostoma ligatum spawns it broadcasts gametes
into the water column. Broadcast spawning is unknown
for other species within this genus. Two other Calliostoma
species produce egg masses or at least attach an egg-bearing
mucous string to the bottom (ROBERT, 1902; LEBOUR, 1937).
Calliostoma ligatum falls between the spawning strategies
of (1) eggs set free singly into the plankton, and (2) eggs
laid in gelatinous layers (PURCHON, 1977) by releasing
eggs in a mucous string. In the laboratory, mucus integrity
broke down and eggs were released into the water column.
It is doubtful that developing larvae would be held in place
by mucus in the field.

The eggs of Calliostoma ligatum obtained here are similar
to those described by HuNT (1980) with the exception of
egg size. Hunt reported eggs being 29-30 um in diameter,
certainly an error. Eggs in the present study were ap-
proximately 225 um in diameter, a size comparable to egg
sizes of C. zizyphinum (280 um) and C. papillosum (170
um) (LEBOUR, 1937).

The development of Calliostoma ligatum differs from
other Calliostoma species that have been described. Other
Calliostoma species bypass a planktic larval stage and hatch
as metamorphosed snails (LEBOUR, 1937) while larvae of
C. ligatum hatch as swimming veligers.

Swimming veligers of Calliostoma ligatum go to the bot-
tom and swim and crawl for 3 to 4 days before metamor-
phosis. It is possible that the duration of the swimming-
crawling stage would be shortened in the presence of a
favorable substrate as has been suggested for other species
(SCHELTEMA, 1961; FRETTER & MANLY, 1977). The abil-
ity to prolong the swimming-crawling stage is advanta-
geous as it allows larvae the time to search for favored
habitats (PECHENIK, 1980). Since clean glass is most likely
not an ideal substrate, larvae in this study show that they
will eventually metamorphose even if an ideal substrate is
not present.

In conclusion, broadcasting gametes and hatching as
planktic larvae places the developmental pattern of Cal-
liostoma ligatum closer to the primitive gastropod pattern
than that of other Calliostoma species whose development
is known.

ACKNOWLEDGMENTS

I thank M. Strathmann, B. Bingham, Dr. L. Cameron,
and Dr. L. F. Braithwaite for providing helpful sugges-
tions pertaining to this project and to B. Bingham for his
willingness to act as a diving partner. I also thank two
anonymous reviewers for their helpful comments. Dr. A.
O. D. Willows provided research facilities at the Friday
Harbor Laboratories. Support for this project came from
research funds allocated by the Department of Zoology,
Brigham Young University, and from a student research
award from the Associated Students of Brigham Young
University.

LITERATURE CITED

CrortTs, D. R. 1955. Muscle morphogenesis in primitive gas-
tropods and its relation to torsion. Proc. Zool. Soc. Lond.
125:711-750.

FRETTER, V. & R. MANLy. 1977. Algal associations of Tricolia
pullus, Lacuna vincta and Certhopsis tubercularis (Gastropoda)
with special reference to the settlement of their larvae. Jour.
Moll. Stud. 57:999-1017.

Hunt, D. E. 1980. Observations on spawning in Calliostoma
higatum (Gould, 1849). Veliger 22:292.

LeBour, M. V. 1936. Notes on eggs and larvae of some Plym-
outh prosobranchs. Jour. Mar. Biol. Assoc. U.K. 20:547-
565.

Lesour, M. V. 1937. The eggs and larvae of the British proso-
branchs with special reference to those living in the plankton.
Jour. Mar. Biol. Assoc. U.K. 22:105-166.

PECHENIK, J. A. 1980. Growth and energy balance during the
larval lives of three prosobranch gastropods. Jour. Exp. Mar.
Biol. Ecol. 44:1-28.

PuRCHON, R. D. 1977. The biology of the Mollusca. Pergamon
Press: Oxford. 560 pp.

RosBerT, A. 1902. Recherches sur le developpement des troches.
Arch. Zool. Exp. Gen., 3rd Ser. 10:269-538.

SCHELTEMA, R. S. 1961. Metamorphosis of the veliger larvae
of Nassarius obsoletus (Gastropoda) in response to bottom
sediment. Biol. Bull. 121:92-109.

The Veliger 30(4):372-376 (April 1, 1988)

THE VELIGER
© CMS, Inc., 1988

Individual Movement Patterns of the Minute Land Snail

Punctum pygmaeum (Draparnaud)

(Pulmonata: Endodontidae)

by

ANETTE BAUR anD BRUNO BAUR

Department of Zoology, Uppsala University, Box 561, S-751 22 Uppsala, Sweden

Abstract.

Movement patterns of the minute land snail Punctum pygmaeum were studied in boxes

provided with natural substrate. Experiments were conducted with different snail densities and box
sizes, but at constant temperature and humidity. The mean displacement per 12 h averaged 47 mm and
was significantly influenced by snail size, but not by box size or snail density. Punctum pygmaeum moved
equal distances at night and during the day. Snails kept in groups showed aggregative behavior. The

adaptive significance of this behavior is discussed.

INTRODUCTION

Movement patterns, and especially distances covered, have
important consequences in determining population size
and genetic structure (cf, DOBZHANSKY & WRIGHT, 1943).
Studies of individual movement patterns in terrestrial gas-
tropods have been concerned mainly with nocturnal activ-
ity and with homing and trail following of large-sized
species (e.g., Helix pomatia Linné [EDELSTAM & PALMER,
1950], Euglandina rosea (Férussac) [CooK, 1985], Limax
maximus Linné [GELPERIN, 1974], Limax pseudoflavus (Ev-
ans) [Cook, 1980]). Little attention has been directed to
movements of minute snail species living in leaf litter (but
see BoaG, 1985). In this paper we report on individual
movement patterns of Punctum pygmaeum (Draparnaud),
the smallest among European land snails.

Punctum pygmaeum occurs in a wide variety of mod-
erately moist habitats, especially in leaf litter of deciduous
forests (KERNEY & CAMERON, 1979). It is one of the most
abundant land snails in Europe, reaching densities of 173
snails/m? (PHILLIPSON & ABEL, 1983). However, little is
known about its life history. Like other endodontoids, P.
pygmaeum exhibits indeterminate shell growth (cf. SOLEM,
1976). It can reproduce in the absence of a mate (BAUR,
1987).

Several hypotheses have been proposed to explain ob-
served movement patterns. Distances traveled have been
assumed to depend on snail density (GREENWOOD, 1974;
OOSTERHOFF, 1977), and they have also been found to
correlate with individual shell size (e.g., Helminthoglypta
arrosa Binney [VAN DER LAAN, 1971], Arion ater (Linné)

[HAMILTON & WELLINGTON, 1981], Monadenia hillebrand
mariposa Smith [SZLAVECZ, 1986]). Asa result of the main-
ly nocturnal activity of land snails, distances traveled at
night may exceed those covered during the day (e.g., Helix
aspersa Miller [BAILEY, 1975], Helix lucorum Linné
[BAILEY & LAZARIDOU-DIMITRIADOU, 1986]). Our exper-
iments were conducted to determine whether distances
moved by Punctum pygmaeum are affected by the size of
experimental containers, snail density, snail size and (or)
time of day. In addition, the spatial distribution of snails
was tested for deviation from randomness.

MATERIALS anp METHODS

Specimens of Punctum pygmaeum were collected in an
aspen (Populus tremula) and birch (Betula spp.) dominated
part of the forest Nasten 5 km SW of Uppsala in central
Sweden (59°50'N, 17°40’E) in September 1986. The snails
were maintained singly on decaying leaves of aspen in
50 x 10 mm petri dishes lined with moist paper towel in
natural daylight at 20-22°C and 90-100% relative hu-
midity. The size of the snails (shell breadth) was measured
to the nearest 0.02 mm using a binocular microscope with
a stage micrometer.

Experimental Design

Movement patterns of Punctum pygmaeum on their nat-
ural substrate were recorded. For this purpose the bottom
of transparent plastic boxes was lined with moist paper
towel covered by a single layer of decaying leaves of aspen.

A. Baur & B. Baur, 1988

Page 373

Since the movements of snails may be constrained by the
size of the container, two different box sizes were used
during the experiments: 12.5 x 9 x 7 cm (small box) and
24.7 x 18 X 7 cm (large box).

To test whether snail density influences movement pat-
terns, experiments were conducted with one or four snails
in each test box. To follow individual behavior, snails were
marked on the shell with minute dots of correction fluid
(“Tipp-Ex’”’). The experiments were conducted under nat-
ural light conditions at 20-22°C. Humidity in the boxes
ranged between 90 and 100%. Snails were randomly as-
signed to different box sizes and snail densities. Each snail
was tested only once, with each test trial lasting 10 days.
Position recordings were made twice a day (0900 and 2100
h). Consequently, 21 positions and 20 displacements were
recorded for each snail. We define movement frequency as
the percent of all displacements where the snails moved 3
mm or more.

Individual movement patterns were recorded for 48
snails. Forty-one of these were collected in the field, and
seven were born in the laboratory.

Statistical Analysis

Data analysis was performed using the SAS program
package (SAS INSTITUTE, INC., 1985). A Mann-Whitney
U-test was applied to test whether snails raised in the
laboratory differed in behavior from those collected in the
field. The influences of box size, snail density, time of day,
and snail size on the distances covered (logarithmic trans-
formed) were evaluated by analysis of variance (ANOVA).
For this analysis snail size was divided into three size
classes. The directions of successive displacements were
tested for independence using x?-test (BATSCHELET, 1981).
The null hypothesis of this test states randomness in the
directions of successive displacements. A runs-test (SOKAL
& ROHLF, 1969:624) was applied to test whether the snails’
behavior showed periodic sequences of activity. Nearest
neighbor distances were calculated for all observations to
determine whether snails tested in groups of four showed
aggregative behavior (CLARK & EVANS, 1954). These dis-
tances were compared with simulated ones (100 runs for
each box size) using t-tests.

Simulated values, based on the assumption of random
dispersion, were obtained by calculating distances between
randomized snail positions.

RESULTS
Displacement

In terms of mean displacement and frequency of move-
ment, snails raised in the laboratory did not differ from
similar-sized ones collected in the field (Mann-Whitney
U-test, both cases P > 0.1). Consequently data of both
groups were pooled for further analyses.

The mean displacements of the snails are summarized
in Figure 1. Since the individuals were not continuously

Table 1

Analysis of variance of the minimal distance traveled by
Punctum pygmaeum in 12 h.

Source of variation d.f. SS F-value IP
Model 14 32.99 5.02 <0.0001
Error 963 451.79
Snail size (S) 2 16.99 18.11 <0.0001
Density (D) 1 0.57 1.21 0.2719
Box size (B) 1 0.14 0.31 0.5799
Time of day (T) 1 0.12 0.26 0.6122
Sx D D 2S Bes y7/ <0.0001
SxB 2 0.74 0.79 0.4553
Syex<aule 2 0.12 0.13 0.8753
Bx D 1 0.22 0.46 0.4986
Bx T 1 1.33 2.84 0.0922
ID) &< “Ie 1 0.02 0.05 0.8225

observed, the values recorded represent minimum distances
traveled over each 12-h period. Mean minimal distances
averaged 47 mm with a range of 3 to 95 mm. This high
variability among individuals can be explained partly by
size, which significantly influenced displacement (Table
1), with larger individuals on average traveling greater
distances (Figure 2). In contrast, box size, snail density,
and time of day had no significant effect on mean dis-
placement (Table 1). These results indicate that Punctum
pygmaeum kept singly or in groups of four in each box
size traveled similar distances within 12 h. However, the
interaction of snail size and density was significant (Table
il).

Representative displacement tracks of two Punctum pyg-
maeum kept singly in large boxes are illustrated in Figure
3. In general, the direction of a given displacement was
independent of the direction of the preceding displacement
(x?-test, all snails P > 0.2, but one P < 0.01).

Timing of Activity

The frequencies of movement for the snails are sum-
marized in Figure 4. Nineteen of the 48 Punctum pyg-
maeum were active during 19 or more 12-h periods, while
16 snails were active during 10-17 periods. The latter
snails, however, showed active sequences of 4-6 consecu-
tive periods interrupted by pauses of 1-3 periods (runs-
test in 12 snails P < 0.01, in four snails P < 0.05). The
remaining 13 snails were irregularly active with no distinct
pattern.

Aggregative Behavior

Significant aggregations of Punctum pygmaeum during
the whole experiment were observed in three of four small
boxes and in two of three large boxes (Table 2). Analysis
of the snails’ positions indicates that in some boxes snails
rested on only a few selected leaves, while in others they

Page 374

10 ZA
: Oo
es _-
3 Zi
7
—_— |

|

0 20 40 80 100
Mean minimum distance (mm)

oa
oO

Figure 1

Distribution of mean displacements for Punctum pygmaeum. Each
value represents the mean of 20 displacements of an individual
snail during 12 h.

showed no preference for any particular leaf. Similar pat-
terns of leaf preference were observed for boxes containing
only one snail.

DISCUSSION
Displacement

Our results showed that individuals of Punctum pyg-
maeum moved approximately 5 cm in 12 h. However, in
the course of a single 12-h period, a snail may actually
travel farther than recorded here. In a pilot experiment,
we monitored the actual tracks of individual Punctum pyg-
maeum creeping on wet paper towels. Stressed by the ar-
tificial light of a 40-W bulb, individual snails moved be-
tween 282 and 480 mm within 40 min (mean for 16
individuals = 407 mm), which corresponded to 6-66% of
their resultant displacement (mean = 29%). Thus, one
may assume that the average distance traveled is about
three times the minimum displacement distance recorded
here. On the other hand, the natural habitat of Punctum
pygmaeum consists of a multiple layer of leaves and, con-
sequently, distances traveled may result in shorter hori-
zontal displacements. Distances covered may also be in-
fluenced by microclimatic factors. In our experiments the
snails were kept under constant temperature and humidity,
as seldom prevail in the field. Undoubtedly, heterogeneity
in microclimate and substrate will influence snail move-
ments under natural conditions.

The positive correlation found between shell size and
distance traveled in Punctum pygmaeum is paralleled in
other snail species (e.g., Helminthoglypta arrosa [VAN DER
LAAN, 1971], Arion ater [HAMILTON & WELLINGTON, 1981],
Monadenia hillebrandi mariposa [SZLAVECZ, 1986]). How-

The Veliger, Vol. 30, No. 4

@
90|- *
@
— @
Ee
E
2 70
(=
{40}
D
5
5
z 50
ie
E
(‘Ss
(40)
(<b)
S 30
e@
e?
e@
e@
10

11 1.2 1.3 1.4 1.5
Shell breadth (mm)

Figure 2

Relationship between mean displacement (y) and shell size (x)
of Punctum pygmaeum (y = 92.4x — 71.7; r = 0.49, n = 45, P
< 0.01).

ever, it seems not to be a general feature of terrestrial
gastropods. For instance, no difference in distances covered
between adults and half-grown juveniles was observed in
Cerion bendalli (WOODRUFF & GOULD, 1980), Arzolimax
columbianus (Gould) (HAMILTON & WELLINGTON, 1981)
and Arianta arbustorum (Linné) (BAUR, 1984, 1986). In
addition to size effects, the high variability in terms of
distances traveled in Punctum pygmaeum may result from
physiological and (or) genetic differences between individ-
uals. Similar individual variation in mobility has been
described for Helix pomatia Linné (LOMNICKI, 1969) and
Arianta arbustorum (BAUR & GOSTELI, 1986).

In our experiments Punctum pygmaeum was kept at
densities ranging from 22 snails/m? (one snail in a large
box) to 356 snails/m? (four snails in a small box), while
the actual density of the original population was estimated
at 63 + 38 snails/m* (mean + SE) in September 1985
(unpublished results). However, we failed to find any in-
fluence of snail density on displacements. In the literature
both density-dependent dispersal (e.g., Cepaea nemoralis
(Linné) [GREENWOOD, 1974; OOSTERHOFF, 1977], Arion
ater [HAMILTON & WELLINGTON, 1981]) and density-in-

A. Baur & B. Baur, 1988

Page 375

Figure 3

Representative displacement tracks of two individuals of Punctum pygmaeum kept singly in large boxes during 21
periods of 12 h. Numbers indicate the sequence of the snails’ positions.

dependent dispersal (e.g., Ariolimax columbianus |[HAM-
ILTON & WELLINGTON, 1981]) have been claimed to occur.

Timing of Activity

In contrast to other studies of gastropods (BAILEY, 1975;
BAILEY & LAZARIDOU-DIMITRIADOU, 1986; ROLLO, 1982;
WAREING & BAILEY, 1985), no distinct differences in ac-
tivity between day and night were found in Punctum pyg-
maeum. In Helix aspersa, for example, 76-92% of the total
activity was observed to take place during the night, with
daytime activity being confined to periods of rainfall
(BAILEY, 1975). The apparent lack of a circadian rhythm

20

Number of snails

LZ

O 20 40 60 80 100
Frequency of movement (% )
Figure 4

Distribution of movement frequencies for Punctum pygmaeum.

observed in Punctum pygmaeum can be an artifact of the
experimental set-up (natural daylight, but constant tem-
perature and humidity), or a trait characteristic of snails
inhabiting leaf litter. The latter suggestion is supported
by findings of BoaG (1985), who described humidity as
the major factor influencing activity of the litter-dwelling
snails Discus cronkhitei’ (Newcomb), Euconulus fulvus
(Miller), Vertigo gould: (Binney), and Vertigo modesta
(Say), while light conditions per se appeared to play a
minor role. Furthermore, snails with distinctly nocturnal
activity and diurnal inactivity, such as Achatina fulica
(Linné), have been shown to retain a circadian rhythm
even when kept under constant high humidity in the lab-
oratory (CHASE ef al., 1980).

Table 2

Aggregative behavior of Punctum pygmaeum. The snails’

dispersion is clumped if the observed nearest neighbor

distances are significantly smaller than the simulated near-

est neighbor distances (based on randomized snail posi-
tions). Distances are given in mm.

Observed
nearest neigh-
bor distance

Simulated
nearest neigh-

; bor distance
Experi-

ment Mean (SD) Mean (SD) t-value P

Small boxes:

I 26.6 (10.2) 35.4 (10.9) 3.44 <0.001
II 32.3 (11.6) 35.4 (10.9) 125 N.S.
Ill 28.1 (9.5) 35.4 (10.9) 2.88 <0.01
IV 28.4 (8.4) 35.4 (10.9) 2.82 <0.01
Large boxes:
I 44.9 (17.7) 65.1 (22.0) 3195000
II 64.2 (24.7) 65.1 (22.0) 0.17 N.S.
Ill 48.9 (17.3) 65.1 (22.0) 3.18 <0.01

N.S. = not significant.

Page 376

Aggregative Behavior

Punctum pygmaeum tended to aggregate. This behavior
might depend upon signals emanating from the animals
themselves, such as pheromones in mucus trails (cf. CROLL,
1983). In fact, P. pygmaeum clustered significantly above
chance level when kept in plastic boxes without environ-
mental stimuli capable of biasing particular locations (un-
published results). However, observations that aggrega-
tions are restricted to particular leaves in some boxes and
not in others, and that snails kept singly tended to rest on
some leaves more often than others, point to the effect of
additional environmental stimuli. Under natural condi-
tions, local concentrations of food (leaves with a high pal-
atability) and high moisture may attract snails. In addition,
the following of mucus trails might contribute to grouping
behavior.

Aggregation is known to occur in several other gastropod
species, but its adaptive significance does not appear to be
the same in every case. In some species aggregative be-
havior may be part of reproductive activities (KUPFER-
MANN & Carew, 1974), while in others it may protect
snails from predation and reduce net water loss by de-
creasing the total surface-volume ratio (CHASE et al., 1980;
Cook, 1981). The adaptive advantage of aggregative be-
havior in Punctum pygmaeum is unknown.

ACKNOWLEDGMENTS

Financial support was received from the Swiss National
Science Foundation and the Ahlstrand Foundation. We
thank Heidi Dobson, Staffan Ulfstrand, and an anony-
mous reviewer for comments on the manuscript.

LITERATURE CITED

BaILEy, S. E. R. 1975. The seasonal and daily patterns of
locomotor activity in the snail Helix aspersa Muller, and their
relation to environmental variables. Proc. Malacol. Soc. Lond.
41:415-428.

BaILEy, S. E. R. & M. LAzARIDOU-DIMITRIADOU. 1986. Cir-
cadian components in the daily activity of Helix lucorum L.
from northern Greece. Jour. Moll. Stud. 52:190-192.

BATSCHELET, E. 1981. Circular statistics in biology. Academic
Press: London. 371 pp.

Baur, B. 1984. Dispersion, Bestandesdichte und Diffusion bei
Arianta arbustorum (L.) (Mollusca, Pulmonata). Ph.D. The-
sis, Zurich Univ. 89 pp.

Baur, B. 1986. Patterns of dispersion, density and dispersal
in alpine populations of the land snail Ar:anta arbustorum
(L.) (Helicidae). Holarct. Ecol. 9:117-125.

Baur, B. 1987. The minute land snail Punctum pygmaeum
(Draparnaud) can reproduce in the absence of a mate. Jour.
Moll. Stud. 53:112-113.

Baur, B. & M. GosTELI. 1986. Between and within population
differences in geotactic response in the land snail Avianta
arbustorum (L.) (Helicidae). Behaviour 97:147-160.

Boac, D. A. 1985. Microdistribution of three genera of small
terrestrial snails (Stylommatophora: Pulmonata). Can. Jour.
Zool. 63:1089-1095.

The Veliger, Vol. 30, No. 4

CHASE, R., R. P. CROLL & L. L. ZEICHNER. 1980. Aggregation
in snails, Achatina fulica. Behav. Neural Biol. 30:218-230.

Ciark, P. J. & F.C. Evans. 1954. Distance to nearest neighbor
as a measure of spatial relationships in populations. Ecology
35:445-453,

Cook, A. 1980. Field studies of homing in the pulmonate slug
Limax pseudoflavus (Evans). Jour. Moll. Stud. 46:100-105.

Cook, A. 1981. Huddling and the control of water loss by the
slug Limax pseudoflavus Evans. Anim. Behav. 29:289-298.

Cook, A. 1985. Functional aspects of trail following by the
carnivorous snail Euglandina rosea. Malacologia 26:173-181.

CROLL, R. P. 1983. Gastropod chemoreception. Biol. Rev. 58:
293-319.

DoBZHANSKY, T. & S. WRIGHT. 1943. Genetics of natural
populations. X. Dispersion rates in Drosophila pseudoobscura.
Genetics 28:304-340.

EDELSTAM, C. & C. PALMER. 1950. Homing behaviour in
gastropods. Oikos 2:259-270.

GELPERIN, A. 1974. Olfactory basis of homing behavior in the
giant garden slug, Limax maximus. Proc. Natl. Acad. Sci.
USA 71:966-970.

GREENWOOD, J. J. D. 1974. Effective population numbers in
the snail Cepaea nemoralis. Evolution 28:513-526.

HAMILTON, P. A. & W. G. WELLINGTON. 1981. The effects
of food and density on the movement of Arion ater and Ario-
limax columbianus (Pulmonata: Stylommatophora) between
habitats. Res. Popul. Ecol. 23:299-308.

KERNEY, M. P. & R. A. D. CAMERON. 1979. A field guide to
the land snails of Britain and north-west Europe. Collins:
London. 288 pp.

KUPFERMANN, I. & T. J. CAREW. 1974. Behavior patterns of
Aplysia californica in its natural environment. Behav. Biol.
12:317-337.

LoMNnIcKI, A. 1969. Individual differences among adult mem-
bers of a snail population. Nature 223:1073-1074.

OOSTERHOFF, L. M. 1977. Variation in growth rate as an
ecological factor in the landsnail Cepaea nemoralis (L.). Neth.
Jour. Zool. 27:1-132.

PHILLIPSON, J. & R. ABEL. 1983. Snail numbers, biomass and
respiratory metabolism in a beech woodland—Wytham
Woods, Oxford. Oecologia 57:333-338.

ROoLLo, C. D. 1982. The regulation of activity in populations
of the terrestrial slug Limax maximus (Gastropoda; Limac-
idae). Res. Popul. Ecol. 24:1-32.

SAS InsTITUTE INc. 1985. SAS user’s guide: statistics. 1985
edition. SAS Inst. Inc.: Cary, North Carolina.

SOKAL, R. R. & F. J. ROHLF. 1969. Biometry. W. H. Freeman
and Co.: San Francisco. 776 pp.

SoOLEM, A. 1976. Endodontoid land snails from Pacific islands
(Mollusca: Pulmonata: Sigmurethra). Part I. Family En-
dodontidae. Field Museum of Natural History: Chicago,
Illinois. 508 pp.

SZLAVECZ, K. 1986. Food selection and nocturnal behavior of
the land snail Monadenia hillebrandi mariposa A. G. Smith
(Pulmonata: Helminthoglyptidae). Veliger 29:183-190.

VAN DER LAAN, K. L. 1971. The population ecology of the
terrestrial snail, Helminthoglypta arrosa Binney (Pulmonata:
Helicidae). Ph.D. Thesis, Univ. Calif., Berkeley. 235 pp.

WakrEING, D.R. & S. E.R. BAILEy. 1985. The effects of steady
and cycling temperatures on the activity of the slug Deroceras
reticulatum. Jour. Moll. Stud. 51:257-266.

WooprurffF, D. S. & S. J. GouLD. 1980. Geographic differ-
entiation and speciation in Cerzon—a preliminary discussion
of patterns and processes. Biol. Jour. Linn. Soc. 14:389-
416.

The Veliger 30(4):377-383 (April 1, 1988)

THE VELIGER
© CMS, Inc., 1988

‘The Gastropods in the Streams and Rivers of Five

Fiji Islands: Vanua Levu, Ovalau, Gau,

Kadavu, and ‘Taveuni

by

A. HAYNES

School of Pure and Applied Sciences, University of the South Pacific,
P.O. Box 1168, Suva, Fiji

Abstract.

Streams and rivers on the islands of Vanua Levu, Ovalau, Gau, Kadavu, and Taveuni,

Fiji, were investigated for gastropods, water conductivity, water hardness, temperature, substrate, and
current speed during 1983 and 1984. As at other Indo-Pacific islands there was a diverse and abundant
lotic gastropod fauna. Twenty-six species were collected on Vanua Levu and 13-16 species were found
in each torrential stream studied on the other four islands. Upstream, above the influence of the tide,
both the longitudinal and horizontal distributions of gastropods appeared to be mainly dependent on
the water speed and type of substrate. A suspected new species of Acochlidium (Opisthobranchia) was

discovered on the island of Vanua Levu.

INTRODUCTION

Land and freshwater mollusks were first collected by
Graeffe from the Fiji islands of Viti Levu, Ovalau, Mo-
tiriki, Ngara, Kadavu, Vanua Balavu, Mago, Kanacea,
and Cikobia-i-lau, and were described by MOuSSON in
1870. More recently the freshwater gastropods on Viti
Levu have been investigated by STARMUHLNER (1976) and
HAYNES (1985) but nothing has been written about gas-
tropods on the other islands since 1870.

This investigation was aimed at finding what freshwater
gastropods were present on the high islands of Vanua
Levu, Ovalau, Gau, Kadavu, and Taveuni. Physical fac-
tors and water chemistry were also measured in order to
see how much these factors contributed to the distributions
of the gastropods.

STUDY AREA

The islands investigated are shown in Figure 1. Vanua
Levu, the second largest island of the group, rises about
1000 m above sea level and has extensive areas on the
northern side where sugar cane is grown, while on the
wetter southern side there are many coconut plantations.

The four smaller volcanic islands (Ovalau, Gau, Ka-
davu, and Taveuni) rise steeply to an altitude of 400-500
m. Their high central regions are covered mainly in rain
forest, while there are many villages and village gardens

containing dalo (Colocasis esculenta), cassava (Manihot es-
culenta), paw paw (Carica papaya), banana (Musa par-
adisiaca), and yoqona (Piper methysticum) in the coastal
areas. Some coconut plantations are found on Ovalau and
Taveuni. The torrential streams on these islands are liable
to sudden flooding and occasionally they become dry in
their lower courses. The substrate of the streams is com-
posed of large rocks and boulders so that the water flows
in a series of short waterfalls, pools, and white cascades.
Macrophytes were absent except 300-400 m upstream
from the mouth at the sides of Naivika Creek, Taveuni,
where watercress (Nasturtium officinale) grew.

All five islands were formed from volcanic eruptions in
Miocene and late Pliocene times while Taveuni is the site
of the most recent (1200 AD) volcanic activity in the Fiji
group (RICKARD, 1966; IBBOTSON, 1961; WoopRow, 1980).

MATERIALS ano METHODS
Vanua Levu

Gastropods were collected from rivers and streams in
October 1983. The stations, 1-10 on the map (Figure 1),
were chosen to be as representative as possible while still
being accessible by road.

The substrate at each station was searched for 30 min
for gastropods. The leaf litter, plants, wood, and upper
and lower surfaces of stones and boulders were inspected

Page 378

The Veliger, Vol. 30, No. 4

FiJ!l ISLANDS
——— |
32 km
TAVEUNI
of )
»
&
ee
Somme
.
MOTIRIKI 1S)
=
>
GAU
NAGARA
Y
BEQA @
ot .'
S é
S}
ms Y
ae
KADAVU
Figure 1

A map of the main islands of Fiji showing the localities of the sampling stations on Vanua Levu and the positions
of the streams that were sampled on Ovalau, Gau, Kadavu, and Taveuni.

and the sand and gravel were sieved. Samples of each
species at all the stations were taken to the laboratory and
identified according to RIECH (1937), STARMUHLNER (1970,
1976), and HAyNEs (1984).

The substrate, water speed, and temperature were noted
and water samples were taken at most stations. The water
samples were analyzed for conductivity (uS) and hardness
(mg CaCO;/L) by the Institute of Natural Resources,
University of the South Pacific.

Ovalau, Gau, Kadavu, and Taveuni

Physical parameters were noted and water samples and
gastropods were collected in 1983-1984 by the methods

described above. A stream on each island was sampled
from the mouth to 2000 m inland at four stations (three
stations on Kadavu). The streams sampled were Rukuruku
Creek, Ovalau; Navure Creek, Gau; Nubulevu Creek,
Kadavu; and Naivika Creek, Taveuni (Figure 1).

Several of each species of gastropod were dissected and
the contents of the guts were examined to find what food
they had been eating.

RESULTS

Specimens of the prosobranchs collected in this survey were
deposited in the Los Angeles County Museum of Natural
History and duplicate specimens are available at the School

A. Haynes, 1988

of Pure and Applied Sciences, University of the South
Pacific, Suva, while specimens of the suspected new species
of Acochlidium were sent to the Vienna Natural History
Museum.

Vanua Levu

The physical and chemical conditions and gastropods
present at each station are shown in Table 1. The no-
menclature of STARMUHLNER (1970, 1976) has been used
where possible. A total of 26 species of gastropods was
found on Vanua Levu, and all except two were proso-
branchs. These exceptions were Physastra nasuta (LACM
83-135.1) (Pulmonata, Planorbiidae) and Acochlidium sp.
(Opisthobranchia, Acochlididae). Of the Prosobranchia,
12 (Neritina pulligera [LACM 84-174.1], N. squamipicta
[LACM 83-139.1], N. auriculata [LACM 84-170.1], N.
turtoni [LACM 83-140.1], N. canalis [LACM 84-171.1],
N. petiti [LACM 84-173.2], N. porcata [LACM 84-168.1],
Neritilia rubida [LACM 83-136.1], Clithon diadema [LACM
83-142.1], C. olivaceus [LACM 83-145.1], C. pritchardi [as
C. corona in HAYNES, 1984] [LACM 83-143.1], C. owa-
laniensis [LACM 84-172.1]) belong to Neritidae, 8 (Me-
lanoides tuberculata [LACM 83-141.1], M. lutosa [LACM
83-145.2], M. plicaria [LACM 83-137.1], M. aspirans
[LACM 83-138.1], Thiara bellicosa [LACM 83-142.3], T.
scabra, T. terpsichore [LACM 83-142.2], 7. amarula
[LACM 83-144.1]) belong to Thiaridae, and 4 (Septaria
lineata [LACM 83-142.4], S. suffreni [LACM 84-174.3],
S. porcellana [LACM 84-173.3], S. sanguisuga [as S. bor-
bonica in Haynes, 1984] [LACM 84-174.2]) belong to
Septariidae (Neritacea).

Physastra nasuta was found only on the northern side of
the island (Stations 1-4, Figure 1), while Acochlidium sp.
was discovered only at Station 6. Station 6 was also where
the greatest number of species (11) were found. In general
more species (6-11) were present in the rivers and streams
on the steeper southern coast compared with those (3-6)
on the flatter more cultivated northern coast (Figure 1).

The values for total ions (916 wS) and hardness (252
mg CaCO,/L) were higher at Station 3 than at any other
station, probably because of nearby limestone rock (RICK-
ARD, 1966). At this station a green sponge encrusted boul-
ders and stones. In the Dreketi-Seaqagqa river system (Sta-
tions 1-4) the temperature (30, 28, 28, 27°C) decreased
as the distance from the sea increased (3, 6, 26, 33 km)
(Table 1).

The temperatures at Stations 8 and 9 were lower than
at other stations probably because measurements were tak-
en earlier in the morning.

In the Dreketi-Seaqaqa river system (Stations 1-4) at
Stations 1, 3, and 4, where the current was between 20
and 40 cm/sec, the gastropods Physastra nasuta, Melanoides
tuberculata, and Neritina pulligera were found (Table 1).
The inland or high altitude species Melanoides lutosa ap-
peared at Station 3 (26 km upstream) and was also present
at Station 4. Septaria porcellana and S. suffreni were present

Page 379

on the boulders at Station 3 but had not reached the stream
at Station 4. The Dreketi River, where Station 2 was
located, was wide and deep and the current slow; conse-
quently, three different gastropods, Thiara_ bellicosa,
Neritilia rubida, and Clithon diadema, were found at this
station (Table 1).

Ovalau, Gau, Kadavu, and Taveuni

The physical and chemical conditions that existed and
the gastropods that were present in the four sampled streams
are recorded in Table 2. The number of species in each
stream was approximately the same. There were 16 species
in Rukuruku Creek, Ovalau, 15 in Navure Creek, Gau,
15 in Nubulevu Creek, Kadavu, and only 14 in Naiviki
Creek, Taveuni, where the calcium content of the water
was low (9 mg CaCO,/L).

Generally the same gastropods were found in the streams
of the four islands. From the mouth to 20 m upstream,
only species that are able to live in brackish water were
present (Table 2). Further upstream (300-400 m) in fairly
swift currents, some of these species persisted, e.g., Clithon
oualaniensis, C. diadema, C. pritchardi, and Septaria por-
cellana. Of these, however, only C. pritchardi and S. por-
cellana were found 1500 m or more upstream (Table 2).
These higher, steeper parts of the streams were rich in
gastropod species (5-11 species) and in numbers of indi-
viduals (up to 125/m?’). Melanoides tuberculata and M.
lutosa were usually found in quieter parts of the stream,
while species such as Clithon olivaceus, C. pritchardi, Ne-
ritina variegata (LACM 84-169.1), and N. canalis were
found on the sides or on the under surface of rocks; the
limpets Septarza spp. were able to live on the upper surfaces
as well as the sides of rocks (Figure 2).

The course of Rukuruku Creek rose less steeply for the
first 500 m than did that of the other three streams. Con-
sequently there was greater diversity of gastropod species
at 300-400 m upstream, because those favoring a less swift
current (e.g., Thiara amarula and Neritina squamipicta)
were able to survive.

When the stomachs of the various gastropod species were
examined they were found to contain mainly unicellular
green algae, diatoms, and filamentous cyanobacteria. Pe-
riphyton scraped from stones on which gastropods had
been found contained similar microphytes.

In the torrential streams investigated, gastropods were
the dominant benthic invertebrates. Insect larvae were ab-
sent from most parts of the streams. Prawns and fish were
present in all streams, especially in pools below cascades.

The temperature, hardness, and total ions in the water
of Rukuruku Creek, Ovalau, and Navure Creek, Gau,
were similar (Table 2) but the water of Nubulevu Creek,
Kadavu, had a slightly higher value for total ions (160
compared with 122 and 147 uS) and was less hard (20 mg
CaCO,;/L compared with 56 and 52). Naivika Creek,
Taveuni, was low in calcium ions (9 mg CaCO,/L) and
total ions (36.1 wS). The temperature was significantly

The Veliger, Vol. 30, No. 4

Page 380

ES

punja210g “5 “pyvauy vi1v}Gag ‘(uossa'T) poom
sisuarupjono uoysy) “bwapoip uoYysny) ‘vsoryjaq «J, ‘asoyoisq.a} DavIy J cL LSC 8¢ 0c-0 uw QS 2B syoor “Joavss LSPOOZ *AO BMA OL
pup}
-12010g ‘§ “nansinsuvs visnjdagy ‘pjpoL0d “NI ‘znpoay ued ‘NV ‘Aqiamog
sypUuD? DUYLaKy ‘SnazvAYO UCYIND ‘subsp “JW “vIDINILAQN) SapLoUv]a|y O01 LS GaSG 0S-0 wy Z sJop[noq 2 sy01 ZSZODA VAD Neseseg 6
pypaur) *§ ‘Duvpjacs0g viunjidag “pjoidiuonbs “xy “oyojnoiunv “Ny “(ZN]99¥) 8r889DA
1UOJIN] DUITLUANT “DUapoIp “D “ypspyoi4d UoYyjy) “DIDINILAqN} SapLoUud]a Al $9 WSC, Ge Ol ul QOS SOO 29 puKs AMY SNOSIGIET UO YIAID 8
pjoidiuonbs
‘N “yoreureyy vypjnoiunp vuyuarny “wpioyonud uoyjn) ‘suvsdsp sapiouvjayyy 9€1 169 82 Ol ul QZ SYOOI 2 Joavss ZHESOA “AD PSOMNAPN = L
nuvjjarL10g °S ‘(2Aa2%f)
pénsinsups viunjdag “pnoxy pyvo10g ‘N ‘znpay 42d ‘Ny ‘Aqiamosg SSEPOA
sypuDs DUYLUaAT “snaIDAYO UOYIYD ‘suDLIdsD “JAI “DIDINILAqQN} SapLoUD]ay\| Or NEC @e O€-Ol Wy LZ SoUO]S ISQATUIA 1¥ “Y PMLYIEN 9
1uaif[ns 5 “vuvjas4.0d mivjidag ‘viadyjnd vurpany ‘(UtYyod)
ipanyonad “-) (Znpogy) snasvayo uoyrj “(pInos) 24oyrtsdaa1 9SIVOA
pivry J, (spulpy) suvudsn ‘(usog) viuv94d “Py “vIvjn24eqN} saprouDjay] 9¢ VILL 82 09-0 Wy8 SOUO}S 2 [BARI cayeqayeqeN ye wieang = ¢
SP DOU ee) £IOCOA -NOATRS
piasyjnd vurjiuan “vsojn) “JW “DIDjNI4aqQn} Saprouvjay “vinsou vLysoshY dN GN ZZ O€-0Z WHEE siapnog ‘sauojs ye “y ebebeag ojur weang +
(znpay) tuasf[ns -g ‘(QuUIT) vuDjja2L0d min} 425 “‘psasyjng ZOPTOA ousny
puyiuany “vjvjno4aqn} ‘JW “(P[NOs)) vsojn) saprouvjayy “vinspu viysvskyg ZSZ S16 82 O¢ Uy 9Z SJOp[Nog 2 souOIs eYNALIeN Jesu yY ebebeag ¢
(znyo 9980DA ‘THeAeqeN
-2Y) Dwepoip voy] ‘(asead) vpiqns vyyiiany “(SpUrFT) 750717]9q vant] Or vIvl 82 Ol TES) Souo}s 2 pues jo jyseo wy C AYMAN = C
(guury) p12syjnd S9CODA
Duiiuany ‘(JI[[NJN]) VIDjNILaqQN] SapiouUDjayy ‘Qapa1oy]) DInsvu v«ysoskyg 9S OPP O€ OFr-O€ WHE $9Uu0}s PY NeyxeIq, OUT yaIaIQ

juasaid spodomsesy (1/0080 (ST) (Oo) (2as/wd) vas Wo.1] ayesqns naa] enurA ‘Q0Q0'0SZ'1 uon
Sul) suor ain} paeds s0ue}sIq ‘gouatajor deul 2 OATY- BIS
ssoupsepy [eioy, -esod = s91VAA
-Wd |,

ee

‘pauTuliajap OU = GN ‘NAT enue, jo puryst ay} UO suole)s Surjduies ay} 1v uasaid spodonses pur ‘sisd[eur 19}eM Jo SiNsot “SUOTITPUCI jeosAyd oy,

I SIE IE

A. Haynes, 1988

Table 2

Page 381

The physical conditions, results of water analysis, and gastropods present at four (three on Kadavu) sampling stations in
a stream on each of the islands of Ovalau, Gau, Kadavu, and Taveuni. ND = not determined.

Mouth-20 m upstream

Current speed (cm/sec)

Temperature (°C)

Hardness (mg CaCO,/L)

Conductivity (uS)
Species

300-400 m upstream

Current speed (cm/sec)

Temperature (°C)

Hardness (mg CaCO,/L)

Conductivity (4S)
Species

1000-1100 m upstream

Current speed (cm/sec)

Temperature (°C)

Hardness (mg CaCO,/L)

Conductivity («S)
Species

Rukuruku Ck.
Ovalau

0-10
26
190
2100
Clithon rarispina
(Mousson), C. prit-
chard, C. diadema, C.

oualaniensis

0-50
DSS)
56
147.1
Clithon oualaniensis, C.
diadema, C. pritchar-
di, Neritina pulligera,
N. canalis, N. squami-
picta, Melanoides as-
pirans, M. plicaria,
M. tuberculata,
Thiara amarula
(Linné), Septaria por-

cellana

0-100
25
58
149.8
Clithon olivaceus, Mel-
anoides lutosa, M.
tuberculata, Septaria
porcellana, S. suffreni

2000 m upstream (side stream)

Current speed (cm/sec)

Temperature (°C)

Hardness (mg CaCO,/L)

Conductivity (uS)
Species

20-40

25

60
5253

Clithon olivaceus,

Melanoides lutosa,
M. tuberculata

Navure Ck.
Gau

0-10
Pil
180
1330
Clithon diadema, C.

oualaniensis

30-40
26
52
122
Clithon diadema, C.
pritchardi, Neritina
turrita (Gmelin), Mel-
anoides aspirans

0-80

D5

55

134

Clithon oliaceus, C.

pritchardi, Neritina
variegata, N. canalls,
N. petiti, N. macgill-
urayi (Reeve), Mel-
anoides aspirans, Sep-
taria porcellana, S.
sanguisuga, S. suffreni

40-60
ND
ND
ND
Clithon olivaceus, Neri-
tina pulligera, N. pe-
titi, N. canalis, N.
variegata, N. porcata,
Septaria porcellana, S.
suffreni, S. sanguisuga

Nubulevu Ck.
Kadavu

0-10
Di,
110
1820
Clithon pritchardi, Neri-
tina auriculata

0-40
26
20
160
Clithon pritchardi, C.
olivaceus, Neritina pe-
titi, N. porcata, Sep-
taria macrocephala
(Guillon), S. porcel-
lana

0-100
26
20
159
Clithon olivaceus, C.
pritchardi, Neritina
variegata, N. canalis,
N. pulligera, Mela-
noides arthuru
(Brott), M. tubercula-
ta, Septaria porcel-
lana, S. suffreni, S.

macrocephala, S. san-
guisuga

ND
ND
ND
ND
ND
ND

Naivika Ck.
Taveuni

0-10
22,
330
6280
Clithon diadema, C.
oualamensis, C. prit-
chardi, Neritina auri-
culata, Septaria por-
cellana

20-30
22
19.67
66.7
Neritina canalis, N.
variegata (Lesson),
Melanoides aspirans,
M. tuberculata, S.
porcellana

50-100
22
9
36.1
Clithon olivaceus, Neri-
tina variegata, Mel-
anoides arthuri, M.
tuberculata, Septaria
suffreni, S. porcel-
lana, S. macrocepha-
la, S. sanguisuga

50-100
21
9.0
36.1
Clithon olivaceus, Neri-
tina variegata, Sep-
taria porcellana

Page 382

The Veliger, Vol. 30, No. 4

Figure 2

The distribution of gastropods across a Fijian torrential stream showing the different habitats of the various shell
types. 1, Melanoides lutosa; 2, Neritina variegata; 3, Septaria porcellana, 4. S. sanguisuga; 5, Clithon olivaceus; 6, C.

pritchard.

lower (21-22°C) than that of the other three streams (25-
27°C) (P < 0.01). Above the brackish water region of the
streams there was little difference in the chemical com-
position along the length of each stream.

DISCUSSION

Twenty-six species of gastropods were found on Vanua
Levu at 10 stations compared with 32 species from 47
stations on Viti Levu (HAYNES, 1985). Species present on
Viti Levu but not found on Vanua Levu were Planorbarius
corneus, Ferrissia noumeensis, Gyraulus montrouzieri, Assi-
minea crosseana, Melanoides arthuru, Fluviopupa pupoidea,
and Fijzdoma maculata. The endemic species Fluviopupa
pupoidea Pilsbry and Fijidoma maculata (Mousson), which
are found in the headwaters of the rivers of Viti Levu,
were not found on any of the five islands. These two species
may be remnants of an old fauna that has survived only
on the geologically older Viti Levu (Lapp, 1934).

Some species (Clithon olivaceus, Neritina variegata, Sep-
taria macrocephala [LACM 84-169.3], and S. sanguisuga)
were absent from all collecting stations on Viti Levu
(Haynes, 1985) but were present on the four smaller
islands. Clithon olivaceus and S. sanguisuga were also found
on Vanua Levu. It is difficult to judge whether these species
have always been absent from streams on Viti Levu or
whether they have recently disappeared because logging
operations have increased the turbidity of the water. Sev-

eral Thiara spp. (e.g., Thiara bellicosa and T. terpsichore)
were found on Vanua Levu and Viti Levu (HAYNES, 1985)
but not in the torrential streams. This was probably be-
cause they have failed to become established in the swift
currents of these streams.

The small (10-15 mm long) shell-less opisthobranch
Acochlidium sp. was found only at Station 6 on Vanua
Levu. It is thought to be an undescribed species and spec-
imens have been sent to E. Wawra, Naturhistorisches Mu-
seum Wien. It is somewhat similar to Acochlidium bayer-
fehlmanni Wawra from the Palau Islands (Wawra, 1980)
and Acochlidium sutter1 Wawra from Sumba, Indonesia
(Wawra, 1979).

A feature of many streams in Fiji is the richness and
abundance of gastropod species. In contrast, islands in the
Caribbean region appear to have many more rheolite insect
species than gastropod species. HARRISON & RANKIN (1976)
found 14 insect species and no gastropod species in high-
level streams (290-488 m altitude) on St. Vincent (Lesser
Antilles) and 15 insect species and 3 gastropod species in
low-level streams (8-274 m altitude). STARMUHLNER &
THEREZIEN (1983) found only one lotic gastropod species
(Neritina punctulata) but over 20 species of insects in streams
on Guadeloupe, Dominica, and Martinique.

However, other islands in the Indo-Pacific region ap-
pear to have a rich gastropod fauna similar to that found
in the Fiji Islands. STARMUHLNER (1982) described 16

A. Haynes, 1988

gastropod species in running water on Andaman Island,
Indian Ocean. These include Melanoides tuberculata, M.
plicaria, Thiara scabra, Neritina pulligera, N. variegata, N.
squamipicta, Septaria porcellana, and Neritilia rubida, which
are also present in Fijian streams and rivers. The mountain
streams of New Caledonia had at least 16 species of gas-
tropods and those of Sri Lanka 13 gastropod species
(STARMUHLNER, 1979).

Likely predators in the slower streams and rivers of
Vanua Levu were odonatid nymphs, coleopterid larvae,
leeches, fishes, and cane toads (Bufo marinus) but in the
torrential streams, because of the scarcity of rheolite in-
sects, the only obvious predators were fish species.

Thiarid species (Melanoides spp. and Thiara spp.) are
viviparous, and almost all are exclusively parthenogenetic,
although a few dioecious populations have been found
(Davis, 1971). Those species (e.g., Melanoides tuberculata
and M. lutosa) that live far inland give birth to juvenile
adults, while species (e.g., M. aspirans and M. plicaria)
that inhabit tidal regions release veligers into the water
(STARMUHLNER, 1976).

The neritid snails (Neritina spp., Clithon spp., and Sep-
taria spp.) are dioecious. After copulation the females lay
eggs in egg cases that they cement to stones, boulders, and
often to shells of other gastropods. It is not known for most
species whether the young hatch as veligers or as juvenile
snails. GOVINDAN & NATARAJAN (1972) reported that eggs
of the lowland Indian species Neritina layardi (Lesson)
hatched as veligers after 20-22 days and those of Septaria
tesselata (=S. lineata Lamarck) hatched as veligers after
14-15 days. ForD (1979) reported that the eggs of the
Hawaiian torrential stream species Neritina granosa Sow-
erby also hatched as veligers. Ford believed that after
hatching the veligers of N. granosa were swept out to sea
and later settled at the mouth of rivers or streams. FORD
(1979) observed long chains of up to 80 young snails (less
than 5 mm high) moving upstream. No such phenomenon
has been observed in Fiji streams but small juveniles (1.5-
2.0 mm high) have been found clinging to the shells of
adult Septaria spp. and Clithon spp. 2 km upstream from
the mouth. These species likely either hatch as juvenile
snails or as veligers that settle in freshwater.

Certain species (e.g., Neritina auriculata, N. turrita, and
Clithon diadema) were confined to brackish or tidal regions
where total ions were high. Above the influence of the tide,
the water speed, and consequently the nature of the sub-
strate, appeared to determine the distribution of gastropods
both along and across the stream. However, it is possible
that the absence of Neritina pulligera and Neritina petiti
from Naivika Creek, Taveuni, was caused by low amounts
of dissolved ions in the water.

ACKNOWLEDGMENT

I thank the Research Committee of the University of the
South Pacific for a grant that made this work possible.

Page 383

LITERATURE CITED

Davis, G. M. 1971. Systematic studies of Brotia costula epis-
copalis, first intermediate host of Paragonimus westermani in
Malaysia. Proc. Acad. Natur. Sci. Phila. 123:53-66.

Forpb, J. I. 1979. Biology of a Hawaiian fluvial gastropod
Neritina granosa Sowerby (Prosobranchia: Neritidae). M.S.
Thesis, University of Hawaii.

GOVINDAN, K. & R. NATARAJAN. 1972. Studies on Neritidae
(Neritacea: Prosobranchia) from peninsular India. Proc. In-
dian Acad. Sci. 38B:225-239.

Harrison, A. D. & J. J. RANKIN. 1976. Hydrobiological stud-
ies of eastern Lesser Antillean islands 2. St. Vincent: fresh-
water fauna—its distribution, tropical river zonation and
biogeography. Arch. Hydrobiol. 2/3(Suppl. 50):275-311.

Haynes, A. 1984. Guide to the brackish and fresh water gas-
tropods of Fiji. Institute of Natural Resources, University
of the South Pacific, Suva. 39 pp.

Haynes, A. 1985. The ecology and local distribution of non-
marine aquatic gastropods in Viti Levu, Fiji. Veliger 28(2):
204-210.

IBBOTSON, P. 1961. The geology of Ovalau, Motiriki and Nain-
gani. Geol. Surv. Dept., Suva, Fiji, Bull. 9:1-7.

Lapp, H.S. 1934. Geology of Viti Levu, Fiji. Bernice P. Bishop
Mus. Bull. 119:1-263.

Mousson, A. 1870. Faune malacologique terrestre et fluviatile
des isles Viti, d’aprés les envois de M. le Dr. Edouard Graeffe.
Jour. Conchol. 18(2):109-135, 179-236.

RICKARD, M. J. 1966. Reconnaissance geology of Vanua Levu.
Geol. Surv. Fiji, Mem. 2:1-81.

RieEcH, E. 1937. Systematiche, anatomische, okologische und
tiergeographische Unterschungen uber die susswassermol-
lusken Papuasiens und Melanesiens. Arch. Naturgesch.
(N.F.) 6(36):40-101.

STARMUHLNER, F. 1970. Die mollusken der Neukaledonischen
binnengewasser. Cah. ORSTOM Ser. Hydrobiol. 4(3/4):
3-127.

STARMUHLNER, F. 1976. Beitrage zur Kenntnis der Susswas-
ser-Gastropoden pazifischer Inseln. Ann. Naturhist. Mus.
Wien 80:473-656.

STARMUHLNER, F. 1979. Distribution of freshwater molluscs
in mountain streams of tropical Indo-Pacific Islands (Mad-
agascar, Ceylon, New Caledonia). Malacologia 18:245-255.

STARMUHLNER, F. 1982. Occurrence, distribution and geo-
graphical range of the freshwater gastropods of the Andaman
Islands. Malacologia 22(1/2):455-462.

STARMUHLNER, F. & Y. THEREZIEN. 1983. Résultats de la
mission hydrobiologique Austro-Francaise de 1979 aux Iles
de la Guadeloupe, de la Dominique et de la Martinique.
Ann. Naturhist. Mus. Wien Part 1A, 85/B:171-218; Part
1B, 85/B:219-262.

Wawra, E. 1979. Acochlidium sutter: nov. spec. (Gastropoda,
Opisthobranchia, Acochlidiacea) von Sumba, Indonesien.
Ann. Naturhist. Mus. Wien 82:595-604.

Wawra, E. 1980. <Acochlidium bayerfehlmanni spec. nov. (Gas-
tropoda: Opisthobranchia: Acochlidiacea) from Palau Is-
lands. Veliger 22(3):215-218.

Wooprow, P. J. 1980. Geology of Kandavu. Bull. 7:1-31.
Ministry of Lands and Mineral Resources, Fiji Government.

The Veliger 30(4):384-386 (April 1, 1988)

THE VELIGER
© CMS, Inc., 1988

New Molluscan Hosts for Two Shrimps and Two

Crabs on the Coast of Baja California, with

Some Remarks on Distribution

by

ERNESTO CAMPOS-GONZALEZ

Escuela Superior de Ciencias, Universidad Autonoma de Baja California,
Apartado Postal 2300, Ensenada, B.C., Mexico

Abstract.

Astraea undosa and Hinnites giganteus are recorded as new hosts for Betaeus harford: and

Pinnotheres margarita respectively. For the latter, a range extension is given to Bahia del Rosario, on
the west coast of Baja California. Atrina tuberculosa is confirmed as a regular host for Pontonia pinnae,
and Protothaca grata and Tagelus affinis as hosts for Pinnotheres reticulatus. The distributional data for
Pinnotheres reticulatus in the Gulf of California are emended, and for Pontonia pinnae a range extension
is given to Laguna de San Ignacio, on the west coast of Baja California Sur.

INTRODUCTION

Some species of decapod crustaceans commonly occur as
symbionts of other invertebrates (PATTON, 1967). On the
coasts of Baja California, some caridean shrimps and pin-
notherid crabs are frequently collected inside, or on, their
hosts (HART, 1964; SCHMITT et al., 1973; WICKSTEN, 1983;
CAMPOS-GONZALEZ, 1986). Recently, the author and some
colleagues collected shrimps of the genera Betaeus and
Pontonia, and two species of crabs, genus Pinnotheres, in
hosts previously not recorded, or overlooked in the recent
literature and now confirmed.

DESCRIPTIONS
ALPHEIDAE
Betaeus harford: Kingsley, 1878

Distribution and hosts: Fort Bragg, Mendocino Co., Cal-
ifornia, U.S.A., to Bahia Magdalena, Baja California Sur,
México; commensal in Haliotis spp. (CHACE & ABBOTT,
1980).

Material examined and new host: 1 male, 1 female, and
3 juveniles, Isla Cedros, Baja California, in the mantle
cavity of Astraea undosa (Wood, 1828), 6 January 1987,
Gabriel Jiménez-Beede, coll.

Remarks: The occurrence of Betaeus harfordi as a com-
mensal of Astraea undosa is apparently rare, since the only
hosts previously recorded are species of Haliotis. ACHE &

DAVENPORT (1972) noted... . “Specifity experiments sug-
gest that B. harford: discriminates a chemical substance or
complex of substances containing sufficient information for
recognizing gastropods of the genus Haliotis from other
.’ It is possible that A. undosa could be a
temporary or occasional host, but more data are necessary
to support this. GHISELIN et al. (1967) found that the amino
acid composition of the shell matrix was similar in Haliotis
and Astraea. It is possible that a putative “host factor”
present in Haliotis may also be present in A. undosa. Lab-
oratory experiments are necessary to resolve this question,
and to determine whether preference is related not only to
the recognition of a chemical substance, but also to mor-

gastropods ...

phology of these hosts.

PALAEMONIDAE

Pontonia pinnae Lockington, 1878

Distribution and hosts: Upper Gulf of California, to Pan-
ama; commensal in Pinna rugosa Sowerby, 1835 (WICK-

STEN, 1983).

Material examined and new hosts: Dozens of males and
females, Bahia de los Angeles, Baja California, commensal
in Pinna rugosa and Atrina tuberculosa (Sowerby, 1835),
summer 1986 and April 1987, Mario Nieves, Alma Rosa
Murillo-Peralta & E. Campos-Gonzalez, colls.; 8 females,
and 1 male, Estero El] Cordon, Laguna de San Ignacio,
Baja California Sur, in ““Callo de Hacha,” 17 May 1987,

Eulogio Lopez, coll.

E. Campos-Gonzalez, 1988

Remarks: WICKSTEN (1983), in her monograph of carid-
ean shrimps of the Gulf of California, noted Pinna rugosa
as the only host for Pontonia pinnae. However, LUKE (1977),
in the catalog of crustacean decapods at the Scripps In-
stitution of Oceanography, also cited this shrimp as oc-
curring on Atrina tuberculosa. My record confirms Luke’s
data. Both Pinna rugosa and A. tuberculosa commonly har-
bor a sexual couple of Pontonia pinnae in the Bahia de los
Angeles area.

PINNOTHERIDAE
Pinnotheres margarita Smith, 1869

Distribution and hosts: Bahia Kino, Sonora, México, to
Panama Bay; commensal in Pinctada mazatlanica (Hanley,
1855), and Argopecten circularis (Sowerby, 1835)
(CAMPOS-GONZALEZ & CAMPOY-FAVELA, in press).

Material examined and new hosts: 4 males and 30 ovig-
erous females, Estero El] Cordon, Laguna de San Ignacio,
Baja California Sur, in Argopecten (?) aequisulcatus (Car-
penter, 1864), 17 May 1987, Eulogio Lopez, coll.; 1 fe-
male, Agua Blanca, Bahia del Rosario, Baja California,
in Hinnites giganteus (Gray, 1825), 4 April 1986, Alfredo
Salas, coll.

Remarks: The females and males collected at Estero El
Cordon agree with the description and variation previously
noted (RATHBUN, 1918; WICKSTEN, 1982; CAMPpos-GON-
ZALEZ & CAMPOY-FAVELA, in press). The female collected
at Bahia del Rosario differed in two features: the carapace
margins are arcuate, whereas they are subangular in the
specimens from Estero El] Cordon and from the Gulf of
California, and the fine pubescence normally present in
the body of this crab is lacking in this female.

Pinnotheres reticulatus Rathbun, 1918

Distribution and hosts: San Felipe, Baja California, to
Costa Rica; hosts, Polymesoda inflata (Philippi, 1851), Pro-
tothaca grata (Say, 1831), and Tagelus affinis (C. B. Adams,
1852) (GLASSELL, 1935; GREEN, 1985).

Material examined: 22 females (2 ovigerous, 2 juveniles),
2 males, Laguna Percebu, about 23 km S of San Felipe,
Baja California, in Protothaca grata and Tagelus affinis,
summer 1986, E. Campos-Gonzalez, coll.; 1 female, Puer-
tecitos, km 72 road San Felipe-San Luis Gonzaga, in P.
grata, August 1986, Gerardo Lopez & E. Campos-Gon-
zalez, colls.

Remarks: Recently GREEN (1985) found that Pinnotheres
jamesi Rathbun, 1923, is a junior synonym of P. reticulatus
Rathbun, 1918. He noted that the distribution of this species
is from off “San Josef Island” Isla San José, Baja Cali-
fornia Sur, to Costa Rica, and recorded Polymesoda inflata
as the only host known. This author, as well as Stas &
ALAGARSWAMI (1967) and SCHMITT et al. (1973), over-
looked the distributional information and new host given

Page 385

by GLASSELL (1935) for this species. Glassell recorded P.
reticulatus from San Felipe, Baja California, living in Pa-
phia grata (=Protothaca grata) and Tagelus affinis. In the
Laguna Percebu area, the prevalence of this pinnotherid
in Protothaca grata is lower. About 1000 clams were dis-
sected to obtain 20 specimens. Only females were found
in this host; juveniles, males, and females were taken inside
T. affinis. Additionally, I have sampled Protothaca grata in
Campo Pescadores (about 2 km N of San Felipe), and
Puertecitos, and found only 1 female in 3000 clams. In
these places I did not find 7. affinis, but the population of
Protothaca grata is greater than at Laguna Percebu. It is
possible that the presence of 7. affinis (“primary host’’) is
necessary for the subsequent infestation of Protothaca grata
(“secondary host”). This phenomenon has been recorded
for Pinnixa littoralis (PEARCE, 1966; GARTH & ABBOTT,
1980).

ACKNOWLEDGMENTS

My great appreciation is due to Gabriel Jiménez-Beede
(Escuela Superior de Ciencias, U.A.B.C.), Alfredo Salas
(Instituto de Investigaciones Oceanologicas, U.A.B.C.), and
Rubén Rios (Centro de Investigacion Cientifica y de Edu-
cacion Superior de Ensenada) for sending me part of the
material recorded. I acknowledge my students, José R.
Campoy-Favela, Gerardo Lopez, Patricia Aleman-Diaz,
Alma Rosa Murillo-Peralta, and Sara Terui-Garcia, for
the invaluable effort and support in my investigations on
commensal crustaceans. I am also indebted to Dr. Mere-
dith Gould (Escuela Superior de Ciencias) and two anon-
ymous reviewers for their comments and criticism of the
manuscript. This work was supported in part by the proj-
ect 038-UABC of the Escuela Superior de Ciencias, Uni-
versidad Autonoma de Baja California.

LITERATURE CITED

ACHE, B. W. & D. DAVENPORT. 1972. The sensory basis of
host recognition on symbiotic shrimps, genus Betaeus. Biol.
Bull. 143:94-111.

CaMpos-GONZALEZ, E. 1986. Records and new host of pea
crabs (Decapoda: Pinnotheridae) for Baja California, Mex-
ico. Veliger 29:238-239.

Campos-GONZALEZ, E. & J. R. Campoy-FAavELa. In press.
Morfologia y distribucion de dos cangrejos chicharo del Golfo
de California (Crustacea, Pinnotheridae). Rev. Biol. Trop.
(Costa Rica).

Cuace, F. A. & D. P. ABBoTT. 1980. Caridea: the shrimps.
Pp. 567-576. In: R. H. Morris, D. P. Abbott & E. C.
Haderlie (eds.), Intertidal invertebrates of California. Stan-
ford Univ. Press: Stanford, California.

GarTH, J. S. & D. P. Asppotr. 1980. Brachyura: the true
crabs. Pp. 593-630. In: R. H. Morris, D. P. Abbott & E.
C. Haderlie (eds.), Intertidal invertebrates of California.
Stanford Univ. Press: Stanford, California.

GHISELIN, M. T., E. T. DEGENS, D. W. SPENCER & R. H.
PARKER. 1967. A phylogenetic survey of molluscan shell
matrix protein. Breviora 262:1-35.

GLASSELL, S. A. 1935. New or little known crabs from the

Page 386

Pacific coast of Northern Mexico. Trans. San Diego Soc.
Natur. Hist. 8:91-106.

GREEN, T. M. 1985. Pinnotheres jamesi synonymized with P.
reticulatus (Decapoda: Brachyura). Proc. Biol. Soc. Wash.
98:611-614.

Hart, J. F. L. 1964. Shrimps of the genus Betaeus on the
Pacific coast of North America with descriptions of three
new species. Proc. U.S. Natl. Mus. 115:431-466.

LuKE,S.R. 1977. Catalog of the benthic invertebrate collection.
I. Decapod Crustacea and Stomatopoda. Scripps Inst.
Oceanogr. Ref. No. 77-9. 72 pp.

PATTON, W. K. 1967. Commensal Crustacea. Proc. Symp. on
Crustacea, Mar. Biol. Assoc. India 2:1228-1243.

PEARCE, J. B. 1966. On Pinnixa faba and Pinnixa littoralis
(Decapoda, Pinnotheridae) symbiotic with the clam Tvesus
capax (Pelecypoda: Mactridae). Pp. 565-589. Jn: H. Barnes
(ed.), Some contemporary studies in marine science. Allen
& Unwin: London.

RATHBUN, M. J. 1918. The grapsoid crabs of America. Bull.
U.S. Natl. Mus. 97:1-461.

The Veliger, Vol. 30, No. 4

RaTHBUN, M. J. 1923. The brachyuran crabs collected by the
U.S. Fisheries steamer “Albatross” in 1911, chiefly on the
west coast of Mexico. Bull. Amer. Mus. Natur. Hist. 48:
619-637.

SCHMITT, W. L., J. C. McCain & E. S. Davipson. 1973.
Decapoda I. Brachyura I. Family Pinnotheridae. Jn: H. E.
Gruner & L. B. Holthuis (eds.), Crustaceorum catalogus.
W. Junk. B.V.: Den Haag. 160 pp.

Sivas, E. G. & K. ALAGARSWAMI. 1967. On an instance of
parasitization by the pea-crab (Pinnotheres sp.) on the black
water clam (Meretrix casta (Chemnitz)) from India, with a
review of the work on the systematics, ecology, biology and
ethology of pea-crabs of the genus Pinnotheres Latreille. Proc.
Symp. on Crustacea, Mar. Biol. Assoc. India 2:1161-1227.

WICKSTEN, M. K. 1982. New records of pinnotherid crabs from
the Gulf of California (Brachyura: Pinnotheridae). Proc.
Biol. Soc. Wash. 95:354-357.

WICKSTEN, M. K. 1983. A monograph on the shallow water
caridean shrimps of the Gulf of California, Mexico. Allan
Hancock Monogr. Mar. Biol. 13:1-59.

The Veliger 30(4):387-394 (April 1, 1988)

THE VELIGER
© CMS, Inc., 1988

Systematics of the Scurriini (New Tribe) of the

Northeastern Pacific Ocean

(Patellogastropoda: Lottiidae)

by

DAVID R. LINDBERG

Museum of Paleontology, University of California, Berkeley, California 94720, U.S.A.

Abstract.

Scurriini, a new tribe of the subfamily Lottiinae Gary, 1840, is proposed for the lottiids

of the Peruvian molluscan province in the southeastern Pacific (Scurria Gray, 1847, species) and
Notoacmea insessa (Hinds, 1842) of the Californian and Oregonian molluscan provinces in the north-
eastern Pacific. Discurria new genus is proposed for N. insessa and the new, early Pleistocene species
Discurria radiata from southern California. Recognition of the relationship between the genera Scurria
and Discurria provides another example of a taxon shared by these two disjunct nearshore marine
regions. The pattern of fossil and Holocene distributions of Scurria and Lottia Sowerby, 1834, in the
eastern Pacific Ocean and Caribbean Sea suggests that migration and later radiations in the family
Lottiidae have proceeded from south to north. This direction is unlike that of many other northeastern
Pacific molluscan taxa that appear to have originated in the northwestern Pacific and migrated into the

northeastern Pacific (west to east).

INTRODUCTION

Discontinuous spatial distributions of marine organisms
are striking and important features in historical biogeog-
raphy. Divisions in the distributions of nearshore marine
molluscan taxa usually reflect prominent geological fea-
tures or areas of geologically recent perturbations (e.g., the
Isthmus of Panama between the tropical eastern Pacific
and the Caribbean Sea and the Wisconsian Glacial Period
prohibiting exchange between the North Pacific and North
Atlantic respectively).

While the absolute time of the event that divided a taxon
can be used to estimate evolutionary or migratory rates,
the pattern that emerges from any analysis is, to a large
extent, dependent on the recognition of phylogenetic re-
lationships between members of the fragmented fauna and
flora (NELSON & PLATNICK, 1981; WILEY, 1981). When
a clade has been divided relatively recently, the subclades
tend to be more similar at lower taxonomic levels (e.g.,
subspecies, species, subgenera) than clades that were sep-
arated earlier. For example, 92 species in 48 shared genera
(about 2:1) occur in both the North Pacific Ocean and
North Atlantic Ocean, separated by the Pleistocene gla-
ciations of Arctic Canada during the last 0.150 Myr (data
from DURHAM & MACNEIL, 1967:330), while only 56

species in 205 shared genera (about 1:4) are in common
between the tropical eastern Pacific and Caribbean, sep-
arated by tectonic activity in Central America during the
last 3.5 Myr (data from VERMEIJ, 1978:269).

The best documented cases of discontinuous distribu-
tions of marine molluscan taxa often involve east-west
divisions (DURHAM & MACNEIL, 1967; VERMEIJ, 1978:
242). However, one of the most intriguing discontinuous
distributions occurs north to south—between the Califor-
nian and Peruvian molluscan provinces along the eastern
Pacific margin.

The faunal and floral similarities between the Pacific
coasts of temperate North and South America have been
well documented in the terrestrial realm (CONSTANCE, 1963;
RAVEN, 1963); GARTH (1957), MARINCOVICH (1973),
WHITE (1986) and others have pointed out relationships
between taxa in the nearshore marine habitats. In a study
of the marine mollusks of Iquique, Chile, MARINCOVICH
(1973) concluded that 49 intertidal genera out of a possible
68 (72%) were common to the Chilean and Californian
provinces. However, Marincovich, like Garth before him,
pointed out that further resolution of the pattern would
require a better knowledge of the systematics of the faunas.
This paper is a contribution towards that goal. Systematics
follow LINDBERG (1986b); see also Table 1.

Page 388

Table 1

Classification of northeastern Pacific Lottiidae.

Nomenclatural
discussion

LINDBERG, 1986b
OLIVER, 1926;
LINDBERG & VER-

Classification

LOTTIIDAE Gray, 1840
PATELLOIDINAE Chapman
& Gabriel, 1923

MEIJ, 1985;
LINDBERG & HICK-
MAN, 1986
LOTTIINAE Gray, 1840 herein
Lottiini Lindberg, new tribe herein

Lottia Sowerby, 1834
Tectura Gray, 1940

Scurriini Lindberg, new tribe
Scurria Gray, 1834

LINDBERG, 1986b
LINDBERG, 1986b
THIEM, 1917; herein
McLEan, 1973;

CHRISTIAENS, 1975b
Discurria Lindberg, new genus herein

SYSTEMATICS
Order Patellogastropoda Lindberg, 1986a
Superfamily Acmaeacea Forbes, 1850
Family LOTTMDAE Gray, 1840

Shell composed of four to six shell layers. Innermost
layer radial and/or complex crossed-lamellar followed by
myostracum, optional radial crossed-lamellar layer, con-
centric crossed-lamellar layer, and prismatic layer(s). Rad-
ula three pairs of lateral teeth, marginal teeth two pairs,
one pair, or lacking. Single gill in nuchal cavity typically
present, but may be absent. Secondary gill in mantle groove
present in some taxa.

Cretaceous to Holocene.

Subfamily LOTTIINAE Gray, 1840

Outer prismatic layer of shell consists of two layers;
ventral portion fibrous prismatic, dorsal surface complex
or simple prismatic. Marginal teeth one pair or lacking.
Single gill in nuchal cavity present, and secondary gill in
mantle groove present in some taxa.

Pliocene to Holocene.

Lottiini Lindberg, new tribe

Prismatic layer predominately fibrous with thin, outer
layer of simple prismatic structure. Marginal teeth one
pair or lacking. Looping of intestine typically simple with
fewer than 3 loops. Secondary gill in mantle groove un-
common.

Distribution: [In the] EASTERN PaciFic: Alaska to Peru.
Age: Pliocene to Holocene.

Discussion: The Lottiini appear to be derived from the
Scurriini by the conversion of the exterior complex pris-

The Veliger, Vol. 30, No. 4

matic layer to simple prismatic and the expansion of the
fibrous prismatic shell layer (see discussion below).

Remarks: Two eastern Pacific genera are referred to this
subfamily, Lottea Sowerby, 1834, and Tectura Gray, 1847.
Members of this tribe predominate in the Aleutian, Or-
egonian, Californian, and Panamic molluscan provinces
(60°N to 5°S).

Scurriini Lindberg, new tribe
“Scurriiden” THIEM, 1917:613.

Prismatic layer predominately complex prismatic with
thin, inner layer of fibrous prismatic structure. Marginal
teeth one pair or lacking. Looping of intestine moderately
complex (<5 loops).

Distribution: EASTERN PAciFic [Disjunct]: Alaska to
southern Baja California; Peru to Chile.

Age: Pliocene to Holocene.

Discussion: The shell structure of members of the Scur-
riini appears to be intermediate between the shell structure
of the subfamilies Patelloidinae Chapman & Gabriel, 1923,
and Lottiinae. In the Patelloidinae the outer shell layer is
a single, uniform prismatic layer. In the Lottiinae the
exterior prismatic shell layer consists of two layers, an
inner fibrous layer and an outer complex or simple pris-
matic layer. The fibrous layer in the Lottiini is typically
thick (about 60% of the prismatic layer) whereas in the
Scurriini it is the thinnest shell layer (less than 20% of
the prismatic layer). The shell structure of the Scurriini
appears to be derived from that of the Patelloidinae by the
differentiation of a fibrous prismatic shell structure from
the ventral portion of the outer complex prismatic layer.

Remarks: Two eastern Pacific genera are referred to this
subfamily, Scurria Gray, 1847, in the southern hemisphere
and Discurria new genus in the northern hemisphere.
Members of the genus Scurria form a diverse patellogas-
tropod fauna in the Peruvian molluscan province (5°40’S
to 42°S) (MARINCOVICH, 1973). The new genus Discurria
occurs between higher latitudes in the northern hemisphere
(25°N to 60°N) and is monotypic in the Holocene of North
America. Both genera have members that are associated
with large intertidal kelps.

THIEM (1917) was the first to recognize the distinctness
of the tribe Scurriini, and diagnosed the “Scurriiden” from
the ‘““Akmaeiden” primarily on gill and shell characters;
he also documented shell structure differences. From his
hierarchical arrangement and “Resultate fur die Phylo-
genie” (translated and reproduced here as Table 2), it is
clear that Thiem considered this taxon to represent a nat-
ural group at the familial level. He further divided the
“Scurriiden” into two subfamily-level taxa, the “Scurri-
ididen” and the “‘Scurriidinen,” distinguishing them from
one another by a suite of alimentary characters.

Thiem’s nominal taxa “Scurriiden,” “Scurriididen,” and

D. R. Lindberg, 1988

Page 389

“Scurriidinen” are vernacular names, and because they
were published after 1900, the names cannot be latinized
and recognized as dating from THIEM’s (1917) publication
[Article 11f (iii) (CZN, 1985)]. In a review of the history
of patellogastropod classification, CHRISTIAENS (1975a) re-
ferred to two of Thiem’s three taxa as Scurriidae and
Scurriinae; however, he did not use or discuss these names
in his classification. Therefore, while Christiaens correctly
latinized ‘Thiem’s names, he did not use them as valid
names for taxa and provided no descriptions or definitions,
and thus they remained unavailable [Article 11d (ii) ICZN,
1985)].

Discurria Lindberg, new genus
Type species: Patella insessa Hinds, 1842.

Shell: Profile medium to high; apex positioned in anterior
one-third of shell. Anterior slope straight to convex, pos-
terior slope convex. Radial and concentric sculpture pres-
ent, typically weak. Exterior color brown with or without
radial markings.

Radula: Lateral teeth unicuspid. Third lateral teeth lateral
to second lateral teeth. Marginal teeth lacking. Ventral
plates complex with strong anterior processes.

Animal: Left gill present in nuchal cavity.

Distribution: NORTHEASTERN PaciFic: Alaska to south-
ern Baja California.

Age: Pliocene to Holocene.
Etymology: di- (dis) apart + scurrza (scurra) jester|’s hat ?]

Remarks: Monotypic in the Holocene, typically associated
with the marine laminarian alga Egregia. Habitats more
generalized in the late Neogene, occurring on hard sub-
strata.

Discurria insessa (Hinds)
(Figures 1-3)
Patella insessa HINDS, 1842:82; pl. 6, fig. 3.

Shell (Figure 1): Profile high; apex positioned in the an-
terior one-third of shell. Anterior slope straight; posterior
and lateral slopes convex. Lateral edges of shell parallel.
Sculpture of fine riblets and concentric growth lines. Apex
dark brown, with or without white markings; remainder
of shell glossy brown. Interior of shell brown. Outcrops
of shell layers along interior margin pronounced. Length,
5-20 mm.

Radula (Figure 2): Lateral teeth approximately equal in
height; second and third lateral teeth broader than first
lateral teeth. First lateral teeth closely set at anterior edge
of ribbon segment, pointed distally, medial edge convex,
lateral edges concave. Second lateral teeth broad, with
straight cutting edge and pointed cusp displaced laterally;

Table 2

Systematics of the Scurriidae sensu THIEM (1917).

English translation of “Resultate ftir die Systematik.”

A. Left neck gill in the nuchal cavity and true gill with lappets
under the mantle edge, interrupted above the head. Radular
formula 1:3-0-3-1; oral fringe around mouth; shell muscle

STN MS, MOSS eet rer reere apse Scurriiden
I. Posterior region of the intestinal coil with single loop of
thressrnvallll Pim tes tim cae eine eae Scurriididen

Referred species: Scurria viridula (Lamarck, 1819), S.
zebrina (Lesson, 1830), S. coffea (Reeve, 1855) [=S.
parasitica (Orbigny, 1841)], S. scabra chilensis Thiem,
1917 [=S. variabilis (Sowerby, 1839)].

II. Posterior region of the intestinal coil with many loops of
the small intestine. Furthermore: pharynxial salivary
glands large and between the intestinal tract. Lappets on
mantle edge much more numerous (as many as 10 per
cm), almost a true gill type Scurriidinen

Referred species: S. scurra (Lesson, 1830), S. apicina
chilensis Thiem, 1917 [=S. scurra].

third lateral teeth not reduced, pointed distally, lateral edge
concave, forming a lateral extension of tooth. Only the
dorsal portions of the lateral teeth are heavily mineralized.
Ventral plates subrectangular with broad, flat anterior
processes. First lateral plates rectangular; second lateral
plates with straight posterior edges and fused with laterally
positioned third lateral plates. Third lateral plates semi-
circular in shape.

Animal: White except for brown pigmentation of dorsal
mantle edge. Snout with encircling oral fringe.

Distribution: ALASKA: Wrangell (56°20'N) to MExIco:
Baja California; Bahia Magdalena (24°30'N) (MCLEAN,
1966:108).

Age: Pliocene to Holocene.

Remarks: The lustrous exterior surface of Discurria in-
sessa has been commented on by DALL (1871) and almost
every subsequent student of northeastern Pacific limpets.
This surface, composed of complex prismatic crystals, and
the convex medial edges of the radular lateral teeth dis-
tinguish D. insessa from all other North American species;
both of these characters serve to unite D. insessa with the
South American Scurria.

Discurria insessa has most recently been assigned to the
genus Notoacmea in systematic accounts of the northeastern
Pacific patellogastropod fauna (CARLTON & ROTH, 1975;
McLEan, 1978; ABBOTT & HADERLIE, 1980; LINDBERG,
1981b). However, as early as 1871 DALL had pointed out
similarities between D. insessa and members of the genus
Scurria including: (1) the coloration patterns of young shells,
(2) the outer, brown shell layers, and (3) the exterior
sculpture. MACCLINTOCK (1967) further commented on
the similar shell structure and protoconch morphologies of

The Veliger, Vol. 30, No. 4

Page 390

\
\\
\
\
\
|
|
|
|
|
|
]
]
|

D. R. Lindberg, 1988

D. insessa and Scurria scurra, the type species of the genus
Scurria. Neither worker commented on the shared char-
acteristic radular lateral tooth shape (Figures 2, 3), and
both gave too much phylogenetic significance to the pres-
ence of the secondary gill in S. scurra. It is now known
that the secondary gill in members of the genus Scurrza is
variable in its development (MCLEAN, 1973), and may be
entirely lacking in some species. Moreover, secondary gills
have arisen in many lottiid taxa and are poor indicators
of phylogenetic relationships (LINDBERG & MCLEAN, 1981;
LINDBERG, 1983 and in press).

Discurria insessa is typically found on the stipes of the
low intertidal laminarian alga Egregia menziesi (Turner)
Areschoug, 1896. However, it also may occur on the shells
of the mussel Mytilus californianus (Conrad, 1837) during
the winter when the stipes of Egregia die back and are
destroyed by winter surf. This has been observed along
the rocky coast line of Santa Cruz County and on San
Nicolas Island, Ventura County, California. At San Nic-
olas Island, what appeared to be the same individual lim-
pets remained present on mussels (in fixed study quadrats)
for up to four months before disappearing. It is not known
whether these limpets subsequently returned to Egregia or
died. Further study of this phenomenon is needed (also
see Choat & Black, 1979).

The association of Discurria insessa with Egregia (and
the resultant characteristic parallel lateral sides of the lim-
pet) has not always been as fixed as it is in the Holocene.
Some Pliocene and Pleistocene specimens of D. insessa have
oval or highly irregular apertures that suggest that this
species occurred on substrata other than Egregza, including
rock and probably mussels (Figure 4).

Regardless of the apparent habitat plasticity seen in
Neogene specimens of Discurria insessa, there is little doubt
that its association with Egregia has been a strong selective
force. The radular morphology of D. insessa suggests this
association. The second lateral teeth with their broad,
straight cutting edges are characteristic of patellogastro-
pods that are associated with marine plants.

The recognition of a closer relationship between Dis-
curria insessa and the Peruvian Scurria rather than with

Page 391

the North American Lottiinae necessitates reconsideration
of ecological work that has been done with this species.
For example, CHOAT & BLACK (1979) compared the life-
history strategies of D. insessa and Lottia digitalis (Rathke,
1833). They reported that D. insessa has a higher growth
rate, greater reproductive effort, and lower age of first
reproduction than L. digitalis. From these findings, and
because of the ephemeral habitat (the stipe of Egregza spp.)
of D. insessa, CHOAT & BLACK (1979:43) concluded that
“selective factors for the development of A. insessa’s life
history may have been the life history characteristics of
Egregia.” Their scenario is consistent with the data, but
the different phylogenetic histories of D. insessa and L.
digitalis complicate this interpretation. Are the differences
in life-history characteristics of these two species the result
of selection operating in different types of environments
as proposed by Choat & Black, or are they different merely
because different lineages of patellogastropods have dif-
ferent life-history characteristics? It is not possible to re-
solve this question from available data, but comparisons
of life-history characteristics of D. insessa with other Scur-
ria species in the Peruvian province could help to resolve
this question.

Between clade comparisons can present problems in in-
terpretation of patellogastropod biological and ecological
literature (Lindberg, in preparation). Sometimes the data
from previous studies needs to be reanalyzed in light of
phylogenetic relationships, and future studies should be
designed to recognize and make comparisons within phy-
logenetic units (.e., clades) first so that trends, constraints,
etc., can be recognized before between clade comparisons
or generalizations are made.

Discurria radiata Lindberg, new species
(Figures 5, 6)
Acmaea sp.: WATERFALL, 1929:checklist.

Shell (Figures 5, 6): Profile medium; apex position sub-
central. Anterior slope concave, posterior slope convex.
Lateral slopes straight. Reconstructed aperture oval.

Explanation of Figures 1 to 8

Figure 1. Discurria insessa Hinds, 1842. Holocene; Santa Cruz,
Santa Cruz County, California. (UCMP Loc. E-756). Scale bar =
10 mm.

Figure 2. Radula of Discurria insessa. a. Lateral tooth mor-
phology. b. Basal plate morphology.

Figure 3. Radula of Scurria scurra (Lesson, 1830). a. Lateral
tooth morphology. b. Basal plate morphology.

Figure 4. Discurria insessa with irregular aperture. Pleistocene;
San Nicolas Island, California; Terrace deposits (UCMP Loc.
D-9614). Scale bar = 10 mm.

Figures 5 and 6. Discurria radiata new species. Holotype, UCMP
Type No. 37530. Early Pleistocene; Saticoy, Ventura County,

California; Saugus Formation (UCMP Loc. 7071). Figure 5:
scale bar = 10 mm. Figure 6: solid light pattern = complex
prismatic outer shell layer; solid dark = fibrous layer; hatched =
concentric crossed-lamellar layer; stippled = radial crossed-la-
mellar layer; irregular, solid light pattern indicates the presence
of matrix. Scale bar = 10 mm.

Figure 7. Radula of Lottza mimica Lindberg & McLean, 1981.
Galapagos Islands. a. Lateral tooth morphology. b. Basal plate
morphology.

Figure 8. Radula of Lottia smithi Lindberg & McLean, 1981.
Galapagos Islands. a. Lateral tooth morphology. b. Basal plate
morphology.

Page 392

Sculpture of concentric growth lines. Exterior color tan
with red-brown radial rays that gently curve from the apex
to the shell margin. Interior of shell white.

Holotype dimensions: Length 12.0, width 8.6, height 6.2
mm.

Type locality: CALIFORNIA: Ventura County [Saticoy
Quad]; Saugus Formation (34°18'N, 119°11’W). About 2
km [1.25 miles] N of mouth of unnamed canyon that lies
1.6 km [1 mile] E of Harmon Canyon, in creek bottom.
Collector: L. N. Waterfall, December 1925 [Museum of
Paleontology, University of California, Berkeley (UCMP)
Loc. 7071].

Age: Early Pleistocene.
Type material: Holotype, UCMP Type No. 37530.

Etymology: radius- Latin noun, ray. Named for the red-
brown radial rays that distinguish this species.

Discussion: Although based on a single specimen, Dis-
curria radiata can be distinguished from other Pliocene,
Pleistocene, and Holocene northeastern Pacific lottiid
species by its shell structure, morphology and color pattern.
Shell structure distinguishes D. radiata from all other
Neogene and Holocene lottiids except Discurria insessa.
Although the gross morphology of D. radiata resembles
that of an oval D. insessa, the radiating red-brown rays
are unique to D. radiata; the only markings found on D.
insessa consist of variable white markings around the apex.

Although less than 75% of the total shell and 50% of
the exterior surface remains on the holotype, there is no
doubt that it is distinct from Discurria insessa. Neogene
specimens of D. insessa are identical to Holocene specimens
in gross morphology and color except for some Pleistocene
specimens that have oval or irregular apertures (Figure
4). The conservative morphology of D. insessa through the
Pleistocene corresponds to the narrow range of variation
present in Holocene specimens. Little morphological vari-
ation is common in limpets that are associated with marine
algae and angiosperms (LINDBERG, 1982 and unpublished
data). Thus, the morphological stability of D. insessa over
the last 1.5-2 million years suggests that it has been as-
sociated with Egregza spp. for this same period of time. In
contrast, the straight sides of D. radiata suggest an oval
aperture and there is no hint of parallel lateral edges. The
reconstructed gross morphology of D. radiata is that of a
rock-dwelling species, not a marine plant species (Figure
6).

The broken and exfoliated shell of the holotype exposes
all four major shell layers of Discurria radiata (Figure
6). The only shell layer not visible to the unaided eye is
the myostracum. The relative thickness of the various shell
layers is similar to that of D. insessa.

Remarks: The Saugus Formation was considered by Wa-
TERFALL (1929) to be either Late Pliocene or Early Pleis-
tocene in age, and the associated fauna warm-water in

The Veliger, Vol. 30, No. 4

character. VALENTINE (1961) suggested that the Plio-Pleis-
tocene boundary in the western Ventura Basin was in the
Pico Formation, which underlies the Saugus Formation.
Thus, the type locality of Discurria radiata, which is
located in the western Ventura Basin, would be Early
Pleistocene in age. Except for D. radiata, the fauna at
UCMP Loc. 7071 (WATERFALL, 1929:checklist) is com-
posed entirely of extant species that occur today along the
central and southern California coast; there are no species
that suggest that thermal conditions were any different
from those of today. The fauna includes such rocky inter-
tidal and shallow subtidal gastropod species as Acanthina
spirata (Blainville, 1832), Margarites lirulata (Carpenter,
1864), and Ocenebra foveolata (Hinds, 1844); soft-bottom
taxa, including the bivalves 77esus nuttalli (Conrad, 1837),
Macoma nasuta (Conrad, 1837), Modiolus rectus (Conrad,
1837), and the gastropods Polinices reclusianus (Deshayes,
1839) and Oliella biplicata (Sowerby, 1825) are also pres-
ent. VALENTINE (1961) concluded that the fossil assem-
blage at UCMP Loc. 7017 represented the Tellina bode-
gensis-Forreria belchert community, which he considered to
indicate a shallow, inner subtidal, chiefly sand-bottom hab-
itat between 0 and 30 m in depth. Discurria radiata was
probably transported into this depositional environment.

DISCUSSION

The recognition of the distinctness and taxonomic affinity
of an incomplete patellogastropod limpet that was collected
60 yr ago was possible because original shell material was
present. The importance of shell structure in patellogas-
tropod systematics has already been demonstrated
(MACCLINTOCK, 1963, 1967; LINDBERG, 1976, 1978, 1979,
1981a, 1983; LINDBERG & MCLEAN, 1981; LINDBERG &
HICKMAN, 1986). Moreover, shell-structure characters can
be used for both fossil and Holocene specimens, and thus
provide data for historical biogeography.

Californian and Peruvian Exchanges

The recognition of the relationship of Discurria insessa
and D. radiata with the Scurriini of the Peruvian province
provides another example of past faunal exchange between
these two physically similar, but disjunct, molluscan prov-
inces. Additional, previously unrecognized, northeastern
Pacific rocky intertidal species that also appear to have
immigrated from the southern hemisphere include: Fis-
surella (Fissurella) volcano Reeve, 1849, the single north-
eastern Pacific representative of a subgenus that is wholly
restricted to the Peruvian province except for two outlying
species (MCLEAN, 1984b), and Fissurellidea bimaculata
(Dall, 1871), the only northeastern Pacific member of a
southern hemisphere group that is distributed from South
America to South Africa (MCLEAN, 1984a).

The genus Discurria first appears in the northeastern
Pacific in the Pliocene of California at San Diego [UCMP
Loc. 5092; San Diego Fm.] whereas Fissurella s.s. and

D. R. Lindberg, 1988

Fissurellidea first occur in the Early Pleistocene of southern
California (GRANT & GALE, 1931). After these initial
appearances, all three taxa quickly become common and
abundant components in later Pleistocene faunas in south-
ern and central California (GRANT & GALE, 1931; VAL-
ENTINE, 1961). It is also during the Pliocene that several
northeastern Pacific taxa (e.g., Chama Linne, 1758; Cren-
omytilus Soot-Ryen, 1955; Cryptomya Conrad, 1848) first
appear in the fossil record of northern Peru (T. DeVries,
personal communication).

The above pattern of Holocene and fossil distributions
and relationships suggests that during the Pliocene and
Early Pleistocene the barriers (e.g., temperature, current
patterns) to faunal exchange between the temperate Cal-
ifornian and Peruvian provinces broke down more than
once and taxa were able to move between the northern
and southern temperate regions by crossing the interme-
diate tropical eastern Pacific. The movement of the Ca-
ribbean plate through the gap between North and South
America (SYKES et al., 1983), and the subsequent regional
perturbations of temperature and currents in the marine
environment (KEIGWIN, 1978, 1982) undoubtedly contrib-
uted to a changing regional setting across which the faunal
exchanges were made.

Scurriini and the Evolution of the Lottiidae

While reviewing THIEM’s (1917) monograph on the
Scurriini, I realized that the endemic Lottia of the Ga-
lapagos Islands combine characters of both the Scurriini
and the Lottiini. These endemic limpets have secondary
gills with morphology similar to those in some members
of the genus Scurria, but their shell structure is identical
to that of Lottia species. Because secondary gills have arisen
several times in different clades in the family Lottiidae
(LINDBERG, in press), the presence of a secondary gill alone
is not strong evidence for considering these species to be
more closely related to the Scurriini than to the Lottiini.
However, the lateral tooth morphology of the endemic
Galapagos species (Figures 7, 8) has previously been seen
only in members of the Scurriini (Figures 2, 3), and there-
fore, the Galapagos species may be more closely related to
the Scurriini than previously thought.

The Galapagos endemics have characters that would
place them in an intermediate position between the genera
Scurria and Lottia, and they are known only from the
Galapagos Islands, which places them directly between the
centers of greatest diversity of both genera. If they are
ancestral to Lottiini, their restriction to the Galapagos
Islands, which have a depauperate Holocene patellogas-
tropod fauna (LINDBERG & MCLEAN, 1981), would mean
that the ancestral group survived in one of the only rocky
intertidal faunas in the eastern Pacific Ocean without Lot-
tia and Tectura species. Alternatively, they could represent
a separate derivation from a different Scurra species.

The presence of the most primitive genus (Scurria) in
the Peruvian province, the presence of possible interme-

Age 99

diate species in the tropical eastern Pacific at the Galapagos
Islands, and the derived genera Lottza and Tectura in the
tropical eastern Pacific, Caribbean, and northeastern Pa-
cific suggest that the direction of migration and later ra-
diations of the Lottiinae may have been from south to
north. This is in contrast to the common pattern of other
molluscan groups that shows taxa originating in the north-
western Pacific and migrating into the eastern Pacific
(MacNeil, 1965; Marincovich, 1984a, b).

ACKNOWLEDGMENTS

I thank E. V. Coan, M. G. Kellogg, and J. H. McLean
for criticism of an early draft of the manuscript, T. DeVries
for discussions of Neogene faunal exchanges between the
Californian and Peruvian provinces, E. V. Coan for no-
menclatural discussions, and M. E. Taylor for preparing
Figure 6.

LITERATURE CITED

AspoTT, D. P. & E. C. HADERLIE. 1980. Prosobranchia: ma-
rine snails. Pp. 230-307. In: R. H. Morris, D. P. Abbott &
E. C. Haderlie (eds.), Intertidal invertebrates of California.
Stanford Univ. Press: Stanford, California.

CARLTON, J. T. & B. RoTH. 1975. Phylum Mollusca: shelled
gastropods. Pp. 467-515. In: R. I. Smith & J. T. Carlton
(eds.), Light’s manual: intertidal invertebrates of the central
California coast. Univ. Calif. Press: Berkeley, California.

CHAPMAN, F. & C. J. GABRIEL. 1923. A revision and descrip-
tion of the Australian Tertiary Patellidae, Patelloididae,
Cocculinidae, and Fissurellidae. Proc. Roy. Soc. Victoria 36:
22-40.

Cuoat, J. H. & R. BLack. 1979. Life histories of limpets and
the limpet-laminarian relationship. Jour. Exp. Mar. Biol.
Ecol. 41:25-50.

CHRISTIAENS, J. 1975a. Revision provisoire des mollusques
marins recents de la famille des Acmaeidae et description de
deux nouveaux sous-genres: Szmplacmaea nov. subgen. et
Collisellacmaea nov. subgen. Inform. Soc. Belge Malacol. 4:
3-18.

CHRISTIAENS, J. 1975b. Revision provisoire des mollusques
marins recents de la famille des Acmaeidae (seconde par-
tie). Inform. Soc. Belge Malacol. 4:91-116.

ConsTANCE, L. 1963. Amphitropical relationships in the her-
baceous flora of the Pacific coast of North and South Amer-
ica: a symposium. Introduction and historical review. Quart.
Rev. Biol. 38:109-116.

DaLL, W. H. 1871. On the limpets with special reference to
the species of the west coast of America, and to a more natural
classification of the group. Amer. Jour. Conch. 6:227-282.

DurRuHAM, J. W. & F.S. MACNEIL. 1967. Cenozoic migrations
of marine invertebrates through the Bering Strait region. Pp.
326-349. In: D. M. Hopkins (ed.), The Bering land bridge.
Stanford Univ. Press: Stanford, California.

Forses, E. 1850. On the genera of British patellaceans. Rept.
Brit. Assoc. Adv. Sci. (1849), Part 2:75-76.

GarTH, J. S. 1957. The Crustacea Decapoda Brachyura of
Chile. Rept. Lund Univ. Chile Exped. 1948-49, 49:1-130.

GRANT, U.S.,IV & H.R. GALE. 1931. Catalogue of the marine
Pliocene and Pleistocene Mollusca of California and adjacent
regions. San Diego Soc. Natur. Hist. Mem. 1:1-1036.

Page 394

Gray, J. E. 1840. Synopsis of the contents of the British Mu-
seum. 42nd ed. Woodfall & Son: London. 370 pp.

Gray, J. E. 1847. A list of genera of Recent Mollusca, their
synonyma and types. Proc. Zool. Soc. Lond. (1847):129-
219.

Hinps, R. B. 1842. Descriptions of new shells. Ann. Mag.
Natur. Hist. 10:81-84.

INTERNATIONAL CODE OF ZOOLOGICAL NOMENCLATURE (ICZN).
1985. International Commission on Zoological Nomencla-
ture (W. D. L. Ride & C. W. Sabrosky, Chairmen). 3rd ed.
Univ. Calif. Press: Berkeley, California. 338 pp.

KEIGWIN, L. D., JR. 1978. Pliocene closing of the Isthmus of
Panama, based on biostratigraphic evidence from nearby
Pacific Ocean and Caribbean Sea cores. Geology 6:630-634.

KEIGWIN, L. D., JR. 1982. Isotopic paleoceanography of the
Caribbean and east Pacific: role of Panama uplift in late
Neogene time. Science 217:350-353.

LINDBERG, D.R. 1976. Cenozoic phylogeny and zoogeography
of the Acmaeidae in the eastern Pacific. Ann. Rept. West.
Soc. Malacol. 9:15-16.

LINDBERG, D. R. 1978. On the taxonomic affinities of Collisella
edmitchelh, a Late Pleistocene limpet from San Nicolas Is-
land, California. Bull. So. Calif. Acad. Sci. 77:65-70.

LINDBERG, D. R. 1979. Problacmaea moskalevi Golikov & Kus-
sakin, a new addition to the eastern Pacific limpet fauna
(Archaeogastropoda: Acmaeidae). Veliger 22(1):57-60.

LINDBERG, D. R. 1981a. Rhodopetalinae, a new subfamily of
Acmaeidae from the boreal Pacific: anatomy and systematics.
Malacologia 20:291-305.

LINDBERG, D. R. 1981b. Invertebrates of the San Francisco
Bay estuary system: Mollusca, family Acmaeidae. The Box-
wood Press: Pacific Grove, California. 122 pp.

LINDBERG, D. R. 1982. A multivariate study of morphological
variation of the limpet Notoacmea depicta (Hinds) and its
synonyms Notoacmea gabatella (Berry) and Notoacmea lepis-
ma (Berry) (Gastropoda: Acmaeidae). Bull. So. Calif. Acad.
Sci. 81(2):87-96.

LINDBERG, D. R. 1983. Anatomy, systematics, and evolution
of brooding acmaeid limpets. Ph.D. Thesis, Biology, Univ.
of Calif., Santa Cruz, California. 277 pp.

LINDBERG, D. R. 1986a. Radular evolution in the Patellogas-
tropoda. Amer. Malacol. Bull. 4(1):115.

LINDBERG, D. R. 1986b. Name changes in the “Acmaeidae.”
Veliger 29(2):142-148.

LINDBERG, D. R. In press. The Patellogastropoda. Malacol.
Rev., Supplement.

LINDBERG, D. R. & C.S. HICKMAN. 1986. A new giant anom-
alous limpet from the Oregon Eocene (Mollusca: Patellacea).
Jour. Paleontol. 60:661-668.

LINDBERG, D. R. & J. H. MCLEAN. 1981. Tropical eastern
Pacific limpets of the family Acmaeidae (Mollusca: Archaeo-
gastropoda): generic criteria and descriptions of six new species
from the mainland and the Galapagos Islands. Proc. Calif.
Acad. Sci. 42:323-339.

LINDBERG, D. R. & G. J. VERMEIJ. 1985. Patelloida chamor-
rorum spec. nov.: a new member of the Tethyan Patelloida
profunda group (Gastropoda: Acmaeidae). Veliger 27(4):411-
417.

MACcCLINTOCK, C. 1963. Reclassification of gastropod Proscu-
tum Fischer based on muscle scars and shell structure. Jour.
Paleontol. 37:141-156.

MacC.inTock, C. 1967. Shell structure of patelloid and bel-
lerophontoid gastropods (Mollusca). Peabody Mus. Natur.
Hist. Yale Univ. 22:1-140.

The Veliger, Vol. 30, No. 4

MacNeliL, F.S. 1965. Evolution and distribution of the genus
Mya, and tertiary migrations of Mollusca. U.S. Geol. Soc.
Prof. Pap. 483-G:G1-G51.

MarINCcOVICH, L., JR. 1973. Intertidal marine mollusks of
Iquique, Chile. Natur. Hist. Mus. Los Angeles Co. Sci. Bull.
16:1-49.

MaRINCOVICH, L., JR. 1984a. Neogene molluscan stages of the
west coast of North America. Palaeogeo., Palaeoclimatol.,
Palaeoecol. 46:11-24.

MaRINCOVICH, L., JR. 1984b. Eastern Pacific molluscan bio-
events and their relation to Neogene planktonic datum planes.
Pp. 69-73. In: N. Ikebe & R. Tsuchi (eds.), Pacific Neogene
datum planes (Contributions to biostratigraphy and chro-
nology). Univ. Tokyo Press: Tokyo.

McLean, J. H. 1966. West American prosobranch Gastro-
poda: superfamilies Patellacea, Pleurotomariacea, Fissurel-
lacea. Ph.D. Thesis, Biology, Stanford Univ., Stanford, Cal-
ifornia. 255 pp.

McLEan, J. H. 1973. Family Acmaeidae. Pp. 18-23. In: L.
Marincovich, Jr., Intertidal marine mollusks of Iquique,
Chile. Natur. Hist. Mus. Los Angeles Co. Sci. Bull. 16.

McLean, J. H. 1978. Marine shells of southern California.
Natur. Hist. Mus. Los Angeles Co., Sci. Ser. 24, Rev. Ed.:
1-104.

McLgan, J. H. 1984a. Shell reduction and loss in fissurellids:
a review of genera and species in the Fissurellidea group.
Amer. Malacol. Bull. 2:21-34.

McLEAN, J.H. 1984b. Systematics of Fissurella in the Peruvian
and Magellanic faunal provinces (Gastropoda: Prosobran-
chia). Natur. Hist. Mus. Los Angeles Co. Contrib. Sci. 354:
1-70.

NELSON, G. J. & N. I. PLATNICK. 1981. Cladistics and vicar-
lance: patterns in comparative biology. Columbia Univ. Press:
New York. 567 pp.

OLIVER, W. R. B. 1926. Australasian Patelloididae. Trans.
Proc. New Zealand Inst. 56:547-582.

RAVEN, P. H. 1963. Amphitropical relationships in the floras
of North and South America. Quart. Rev. Biol. 38:151-177.

SOWERBY, G. B. 1825-1834. The genera of Recent and fossil
shells. Vol. 2. London. Plates 127-262 and text; pages not
numbered.

Sykes, L. R., W. R. McCann & A. L. Karka. 1982. Motion
of Caribbean plate during the last 7 million years and im-
plications for earlier Cenozoic movements. Jour. Geophy.
Res. 87(B13):10656-10676.

TuHiEM, H. 1917. Beitrage zur Anatomie und Phylogenie der
Docoglossen; II, Die Anatomie und Phylogenie der Mono-
branchen (Akmdaiden und Scurriiden nach der Sammlung
Plates. Jenaische Zeitschr. Naturw. 54:405-630.

VALENTINE, J. W. 1961. Paleoecologic molluscan geography
of the California Pleistocene. Univ. Calif. Pub. Geol. Sci.
34:309-442.

VERMEIJ, G. J. 1978. Biogeography and adaptation. Harvard
Univ. Press: Cambridge, Massachusetts. 332 pp.

WATERFALL, L. N. 1929. A contribution to the paleontology
of the Fernando Group, Ventura County, California. Univ.
Calif. Publ. Bull. Dept. Geol. Sci. 18(3):71-92.

Waite, B. N. 1986. The isthmian link, antitropicality and
American biogeography: distributional history of the Ath-
erinopsinae (Pisces: Atherinidae). Syst. Zool. 35(2):176-194.

WILEY, E. O. 1981. Phylogenetics. The theory and practice of
phylogenetic systematics. John Wiley & Sons: New York.
439 pp.

The Veliger 30(4):395-399 (April 1, 1988)

THE VELIGER
© CMS, Inc., 1988

Anatomy and Zoogeography of Glossodoris sedna and

Chromodoris grahami (Opisthobranchia: Nudibranchia)

in the ‘Tropical Western Atlantic and Caribbean

HANS BERTSCH

Biological Sciences, National University, 8 Executive Park Circle,
Irvine, California 92714, U.S.A.

Abstract. The eastern Pacific Glossodoris sedna is reported from the tropical western Atlantic Ocean,
and the range of Chromodoris grahami is extended throughout the extremes of the Caribbean Sea. The
anatomies of the specimens are described and compared with original and subsequent descriptions of

these species.

The following records are significant range extensions
for two species of Chromodorididae.

Glossodoris sedna (Marcus & Marcus, 1967)
(Figures 1-2, 5-9)

Synonymy and references: The synonymy and tropical
eastern Pacific distribution of Glossodoris sedna have been
summarized by BERTSCH (1978b) and RUDMAN (1984).

Material examined: Two specimens (Figures 1, 2), 65
mm long; 2 m depth, Tavenier Key, Florida (approx.
25°01’N, 80°30'W); leg. Barry Hamann, 7 June 1983.
Specimen A, radula illustrated in Figure 9, is deposited
in the collections of the Los Angeles County Museum of
Natural History (Malacology), LACM 83-147. Specimen
B, radula illustrated in the scanning electron micrographs
of Figures 5-8, has been deposited in the collections of the
California Academy of Sciences, Department of Inverte-
brate Zoology and Geology, CASIZ 064510.

Photographic records: One specimen, Biscayne Bay,
Florida; photo by Bill Lyons. One specimen, Pennekamp
State Park, off Key Largo, Florida; photo by Roy Manstan,
published on the cover of Sea Frontiers, March-April 1980.

This is the first report of Glossodoris sedna in the tropical
western Atlantic.

External morphology: The coloration of the animals was
white (or a dirty gray white), with two marginal bands:
an inner red and an outer yellow band. Identically colored
bands were also on the underside of the ruffled mantle
margin and around the base of the foot. Gills and rhino-

phores were tipped with pinkish red. There are prominent
folds and crenulations of the mantle margin. These pat-
terns are nearly identical with those seen in typical Glos-
sodoris sedna from the Gulf of California.

The only differences in external morphology between
the Caribbean and Gulf of California animals were the
shade of whiteness and the amount of crenulations. The
specimens collected at Tavenier Key (Figures 1, 2) are a
light grayish white (not the pure white that is usually seen
in eastern Pacific specimens); moreover, they have far more
crenulations in the mantle margin (12 or more) than are
usually present in eastern Pacific animals. The coloration
is only a shading difference, easily variable by dietary
differences; it is not a significant color difference (e.g., blue
vs. green or red vs. yellow). The crenulations are known
to vary within and between individuals and species of
Glossodoris. RUDMAN (1986:132, figs. 20F-H) illustrated
three different individuals of G. rufomarginata (Bergh, 1905)
with single, few, or many crenulations. The Florida animal
illustrated in Sea Frontiers (MANSTAN, 1980) had fewer
crenulations than the specimens from Tavenier Key, more
closely matching the crenulation pattern shown in the orig-
inal drawing of G. sedna (Marcus & Marcus, 1967:179,
fig. 34).

Internal morphology: The reproductive system matched
that described by Marcus & Marcus (1967:179-180).
The morphology of the penis and vas deferens, and the
arrangement and relative size of the vagina, insemination
duct, bursa copulatrix and receptaculum seminis, are all
identical.

The radular formula of specimen A from Tavenier Key

Page 396

The Veliger, Vol. 30, No. 4

Explanation of Figures 1 to 4

Figures 1 and 2. Living animals of Glossodoris sedna, 65 mm long,;
collected at Tavenier Key, Florida. Photo by Jeff Hamann.

Figure 3. Living animal of Chromodoris grahami from Kingston
Harbor, St. Vincent, 20 mm long. Photo by Jeff Hamann.

was 133 (54.1.54). The innermost tooth in each half row
had denticles on both sides of the cusp (2 on the inside
and 3 or 4 on the outer face). The rest of the teeth in each
half row had 4-6 small denticles on the outer side of each
cusp, but the outermost 10 teeth lacked these accessory
denticles on the cusp (Figure 9).

The radular formula of specimen B from Tavenier Keys
(Figures 5-7) was 128 (49.1.49). The innermost lateral

Figure 4. Living animal of Chromodoris grahami from La Par-
guera, Puerto Rico. Photo by C. E. Cutress.

tooth of each half row had 3 or 4 inner and 4 or 5 outer
denticles on the sides of the cusp (Figure 7). The outer
lateral teeth had 6-8 denticles on the outer side of the cusp
(Figure 6), except the outermost 19-21 teeth which were
smooth (Figure 5). The jaw elements (Figure 8) are bifid;
however some are trifid and there are several small ac-
cessory points on a few of the elements.

The holotype of Glossodoris sedna had a radular formula

Explanation of Figures 5 to 8

Scanning electron micrographs of the radula and jaws of Glos-
sodoris sedna, specimen A, collected at Tavenier Key, Florida.
SEMs by author.

Figure 5. Outermost marginal teeth.

Figure 6. Teeth from center of half row.

Figure 7. Rachidian and innermost lateral teeth.

Figure 8. Bifid jaw elements.

H. Bertsch, 1988 Page 397

.o 4 * Fa P § a Se ,
AG f 5 f j J C-
\ 2 ba })
yj ¥ /
¥
f % 4
t 7 ,
f poe i :
P@ ; IF
: ae * ay & oe >
\ F \ie
j \
J a ‘
= if \
7 ¥

iSkKY 8250" doom I 232616 15Ky

@32617 15KY 4508 68um

Page 398

A

Figure 9

Sketches of radular teeth of Glossodoris sedna, specimen B, of
Tavenier Key. A. Smooth outer marginal, posterior quarter of
radula. B. Rachidian tooth. C. Denticulate lateral tooth from
near the middle of the half row, one-third of the distance from
the anteriormost end of radular ribbon.

of 130 (55.1.55); the innermost lateral tooth had 1 or 2
inner and about 5 outer denticles; the succeeding laterals
had up to 7 denticles; and the outermost 25-35 teeth were
smooth (Marcus & Marcus, 1967:180). The numerical
counts of the Florida specimens closely match those of the
holotype, and fall completely within the range of variation
of the Gulf of California specimens described in the data
and regression analyses of BERTSCH (1978b:71-76). The
tooth shapes illustrated in Figures 5-7 match well those
illustrated by BERTSCH (1978a:figs. 47-50).

The internal anatomy of the Florida animals is identical
with that described for Gulf of California animals. The
external anatomy is very similar (the only differences being
a grayer body and more marginal ruffles). Given the over-
whelming similarities, these differences are not sufficient
to erect a new taxon. It is far more biologically reasonable
to consider these west Atlantic specimens as Glossodoris
sedna, with a slight variation of body tone and a tendency
to more crenulations; this amount of morphological vari-
ation is certainly not unexpected and is consistent with the
geographic separation and isolation of the population.

Zoogeography: This tropical eastern Pacific species is
very common throughout the Gulf of California and along
the Pacific coast of Mexico and Central America to the
Galapagos (BERTSCH, 1978b). Numerous other species of
nudibranchs are known to occur in both the Pacific and
Atlantic (Caribbean) coasts of the tropical Americas (e.g.,
BERTSCH, 1979; GOSLINER & BERTSCH, 1985). However,
Glossodoris sedna is unique in that its known western At-
lantic occurrences are only from the southern tip of Florida,
not throughout the various islands of the Caribbean. Curi-
ously, the three Florida localities are all within 75 km of
each other.

Chromodoris grahami Thompson, 1980
(Figures 3, 4, 10)

Material examined: One specimen, 8 mm long, 4 mm
wide; shallow subtidal, Iron Castle Point, Porto Bello,

The Veliger, Vol. 30, No. ar

B Cc
Figure 10

Sketches of radular teeth of Chromodoris grahami, specimen col-
lected at Panama. A. Strongly curved innermost lateral tooth. B.
Second lateral tooth, row 18. C. Elongate, pectinate condition of
tooth from center of half row, tooth row 9.

Panama (9°33'30"N, 79°40'45”W); leg. H. Bertsch, 22
September 1974. Deposited in the collections of the Los
Angeles County Museum of Natural History (Malacol-
ogy) LACM 74-104.

Photographic records: One specimen, 20 mm long; shal-
low water 1 m deep, Kingston Harbor, St. Vincent (ap-
prox. 13°9'N, 61°14'W); leg. Jeff Hamann, January 1987
(Figure 3).

One specimen, La Parguera, Puerto Rico (approx.
17°58'N, 67°03’W); leg. Charles E. Cutress, December
1983 (Figure 4).

Prior to this study, Chromodoris grahami had been re-
ported in only its original description.

External morphology: The dorsal color of the animals
found at St. Vincent (Figure 3) and at Puerto Rico (Figure
4, shown on a pinkish red sponge) was a cloudy salmon
pink with three irregular rows of bright red spots. The
color bands around the rims of the mantle and foot were
different. The specimen from Puerto Rico had only a white
band, whereas the St. Vincent animal had an outer yellow
line encircling the notum, inside of which was a very thin
red line, which in turn enclosed a broad white band.
THOMPSON (1980) described only yellow and white mar-
ginal bands.

The animal from Panama was pinkish red with darker
red spots irregularly placed over the dorsum, and a prom-
inent whitish marginal band around the notum. The rhino-
phores and gills were also pinkish red, with tinges of white
at the tips or edges. This specimen also did not have the
yellow and white mantle margin bands reported by
THOMPSON (1980). It exhibited an inner cream-white band
and an outer translucent edge around the margin of the
mantle.

These three specimens show a small range of variation
from the coloration originally described in the mantle mar-

H. Bertsch, 1988

gin. However, common to all known Chromodoris grahami
is the fairly broad white band encircling the animal, with
a salmon-pink dorsal color mottled with three rows of
bright red spots.

Internal morphology: The radular formula of the spec-
imen from Panama was 39 (26-27.0.26-27), similar to
the 36 (23.0.23) formula reported by THOMPSON (1980:
80). The innermost lateral tooth (Figure 10A) was strongly
recurved (with 4 or 5 accessory denticles visible), while
the outer laterals are more elongate (Figure 10B), ap-
proaching a pectinate condition (Figure 10C), as reported
by THOMPSON (1980:80-81, fig. 5C).

Except for the slight variation in mantle margin col-
oration, these animals closely match the original descrip-
tion of Chromodoris grahamu.

Zoogeography: The specimen from Panama represents a
southern range extension of over 900 km, and the Puerto
Rican and Lesser Antillean records are eastward range
extensions of over 1000 and 1700 km respectively, from
the only previously reported occurrence of Chromodoris
grahami in Jamaica (approx. 18°N, 77°30’W). Chromodoris
grahami is now known from four widely scattered Carib-
bean extremes (Panama, Jamaica, Puerto Rico, and St.
Vincent). This species can be considered a shallow-water
endemic throughout the Caribbean Sea.

ACKNOWLEDGMENTS

I thank Mr. Jeff Hamann, of El Cajon, California, for
generously allowing me to use his and his family’s collec-

Page 399

tion data and his photographs; and Dr. Cutress for the use
of his photo. A grant from the Smithsonian Tropical Re-
search Institute enabled me to study and collect opistho-
branchs in Panama; and Dr. Terrence Gosliner, of Cal-
ifornia Academy of Sciences, kindly provided me use of a
scanning electron microscope.

LITERATURE CITED

BERTSCH, H. 1978a. The Chromodoridinae nudibranchs from
the Pacific coast of America. Part II. The genus Chromodoris.
Veliger 20(4):307-327.

BERTSCH, H. 1978b. The Chromodoridinae nudibranchs from
the Pacific coast of America. Part III. The genera Chromo-
laichma and Mexichromis. Veliger 21(1):70-86.

BERTSCH, H. 1979. Tropical faunal affinities of opisthobranchs
from the Panamic province (eastern Pacific). Nautilus 93(2-
3):57-61.

GOSLINER, T. M. & H. BERTSCH. 1985. Records and mor-
phology of Lomanotus stauber: Clark & Goetzfried, 1976,
from the Panamic Pacific. Veliger 27(4):397-405.

MANSTAN, R. 1980. Cover photograph. Sea Frontiers 26(2).

Marcus, Ev. & Er. Marcus. 1967. American opisthobranch
mollusks. Univ. of Miami, Studies in Tropical Oceanogra-
phy 6:viii + 256 pp.

RupMAN, W. B. 1984. The Chromodorididae (Opisthobran-
chia: Mollusca) of the Indo-West Pacific: a review of the
genera. Zool. Jour. Linn. Soc. 81(2/3):115-273.

RupMaNn, W. B. 1986. The Chromodorididae (Opisthobran-
chia: Mollusca) of the Indo-West Pacific: the genus Glos-
sodoris Ehrenberg (= Casella H. & A. Adams). Zool. Jour.
Linn. Soc. 86:101-184.

Tuompson, T. E. 1980. Jamaican opisthobranch molluscs II.
Jour. Moll. Stud. 46(1):74-99.

THE VELIGER

© CMS, Inc., 1988
The Veliger 30(4):400-407 (April 1, 1988)

A New Fossil Cypraea (Gastropoda: Prosobranchia) from

Southern Africa with Notes on the Alexandria Formation
by

WILLIAM R. LILTVED

Department of Invertebrate Zoology, California Academy of Sciences, Golden Gate Park,
San Francisco, California 94118, U.S.A.

AND

Id, (Gi, Ibis INU

Geological Survey, P.O. Box 1774, Port Elizabeth 6000, South Africa

Abstract. A new extinct species of Cypraea, C. zietsmami, is described from the Neogene of the
Alexandria Formation from the eastern Cape Province of South Africa. It is compared with allied

Recent and fossil taxa. The depositional environments and associated fauna are described.

INTRODUCTION

In June 1981, Ross Zietsman, of the Port Elizabeth City
Engineers Department, collected a number of fossil gas-
tropod and bivalve shells while excavating in the Neogene
Alexandria Formation near Port Elizabeth, in the eastern
Cape Province of South Africa. The collection included an
undescribed species of Cypraea. Additional specimens per-
taining to the new species were collected by the South
African Geological Survey, during further investigation of
the Alexandria Formation in 1985 and 1986. This paper
describes the aforementioned taxon and gives a generalized
summary of the Alexandria Formation and fauna asso-
ciated with it.

DESCRIPTION
Cypraea zietsmani Liltved & Le Roux, sp. nov.
(Figures 1-3, 5 in part)

Shell large, 56-66 mm in length, depressed, pyriform.
Margins broad, angularly rounded, corrugate, especially
posteriorly, and deeply cut by wide posterior notch. Dorsal
surface bears two heavily calcified tubercles in posterior
one-third of shell, one on either side of medio-dorsal line.
Less eroded shells possess a short dorsal sulcus between

raised thickened ridges immediately adjacent to the medio-
dorsal line. Sulcus situated on pronounced dorsal hump at
one-third anteriorly. Hump slopes abruptly toward pro-
duced anterior terminal. Base heavily thickened, flattened,
with distinct depression along columellar peristome. Mar-
gins reflected on either side, extending beyond lateral plane
of body whorl in mature individuals. Aperture moderately
narrow, slightly curved, constricted posteriorly by funic-
ular callus. Medial portion of aperture evenly wide, be-
coming dilated anteriorly. Columellar peristome poorly
defined owing to concave basal depression, edentate for
most of its length, except for up to five coarse, uneven,
rounded teeth situated above the fossula. Fossula flared,
concave, edentate, with prominent terminal ridge extend-
ing concavely upward into flattened columellar flange,
which borders the anterior siphonal canal. Labrum broad,
widest posteriorly, becoming narrower anteriorly, with 15
to 20 coarse, evenly spaced, rounded teeth present along
inner edge. Teeth extend as raised ridges to two-thirds of
labral width. The type specimens are predominantly chalky
white and lack any color. Under ultraviolet light, how-
ever, the raised transverse labral ridges are pigmented and
the columellar portion of the base shows transverse bands
and spots (Figure 3). Pigment spots are present on the
margins within recessed portions of the posterior corru-
gations, and wide zig-zag markings are present anteriorly.

W. Liltved & F. G. Le Roux, 1988

Page 401

Figure 1

Cypraea zietsmani Liltved & Le Roux, sp. nov. Holotype shell, 58.6 mm long. Left, dorsal; middle, ventral; and

right, lateral aspects.

Measurements:
Length Width Height
(mm) (mm) (mm)

Holotype

(SAM-PQ

2573) 58.6 38.5 26.4
Paratype F

(SAM-PQ

2574) 65.8 50.4 30.9
Paratype H

(SAM-PO

2575) 63.8 46.6 28.6
Paratype G

(CASG-

61612.01) 62.7 48.8 28.8
Paratype A

(LR 263) 56.8 39.9 26.5
Paratype B

(LR 270) 56.0 45.0 Pe)
Paratype C

(LR 265) 60.8 47.1 30.9
Paratype D

(LR 271) 58.0 46.1 27.4
Paratype E

(LR 267) 59.8 49.5 28.9

Type locality: Aloes Siding, 15 km north of Port Elizabeth
(33°48'56"S, 25°37'49”"E), eastern Cape Province, South
Africa, Pliocene, Alexandria Formation, 44 m elevation,
pebbly calcareous sandstone.

Type deposition: The holotype (SAM-PQ 2573), and
two paratypes (SAM-PQ 2574, 2575) have been deposited
in the South African Museum. The three aforementioned
specimens were collected at the type locality by Ross Ziets-
man in June 1981. Five paratypes (LR 263, 265, 267,
270, 271) have been deposited in the collection of the
Geological Survey, South Africa. These five paratypes were
collected by the Geological Survey at St. George’s Strand
north of Port Elizabeth, in 1985 and 1986. One paratype
(CASG-61612.01) has been deposited in the California
Academy of Sciences. This specimen was collected at the
type locality by Ross Zietsman in June 1981.

Discussion: Cypraea zietsmani sp. nov. conchologically
most closely resembles the Recent species C. fultoni Sow-
erby, 1903, which occurs at depths exceeding 65 m off the
coast of Natal, South Africa. The major difference in shell
morphology between the two is that C. ztetsmani invari-
ably lacks the columellar dentition of C. fultoni. Cypraea
zietsmam may possess up to five rounded teeth along the
anteriormost portion of the columellar peristome imme-
diately above the fossula, but otherwise is edentate. The
columellar peristome of C. zietsmani is poorly defined
owing to the innermost portion of the columellar basal
area being recessed and relatively thin, whereas that of C.
fultoni is heavily callused with a well-defined, toothed col-
umellar peristome. All examined specimens of C. ztets-
mani possessed two pronounced, posteriorly situated dor-
sal tubercles. Some of the less eroded shells displayed a
clear, short dorsal sulcus, situated anteriorly, between
thickened ridges, immediately on either side of the medio-

Page 402

The Veliger, Vol. 30, No. 4

Figure 2

Cypraea zietsmant. Shell from collection of Mrs. F. Ball, 60.5 mm long. Left, dorsal; middle, ventral; and right,

lateral aspects.

dorsal line. Neither of these characters is present in C.
fultoni. However, similar tubercules may be seen on the
shells of extinct and extant congeners. Cypraea mus Linné,
1759, a living shallow-water species from Venezuela and
Colombia, and ancestral species belonging to the C. he-
nekeni Sowerby, 1850, complex (INGRAM 1947, 1948) from
the Mio-Pliocene of South and Central America, exhibit
similar dorsal tuberculations to those found on shells of C.
zietsmam. Cypraea teulere: Cazenavette, 1845, a recent,
shallow-water species from the Gulf of Oman is also con-
chologically similar to C. fultoni and C. zietsmani, but is
virtually edentate and lacks any vestige of dorsal tuber-
culations. The three extant relic species, C. fultoni, C. mus,
and C. teuleri, extinct species such as C. zietsmamni, and
members of the C. henekenz complex (C. andersoni Ingram,
1947, C. caroniensis Maury, 1927, C. cayapa Pilsbry &
Olsson, 1941, C. grahami Ingram, 1947, C. henekeni Sow-
erby, 1850, C. isthmica (Schilder, 1927), C. merriami In-
gram, 1939, C. nowele: Maury, 1917, C. projecta Ingram,
1947, C. quagga (Schilder, 1939), C. rugosa Ingram, 1947,
and C. tuberae Ingram, 1948) appear to be related. All of
these species are characterized by being somewhat squat
with a pronounced dorsal hump situated in the posterior
one-third of the shell. The bases are typically flat and
broad with centrally placed apertures. The margins are
deeply cut posteriorly by a wide notch. The fossula ter-
minates in a well-formed terminal ridge, and is normally
devoid of denticles. Recent species are characterized by
having a rather amorphous dorsal color pattern. Well pre-
served fossil material viewed under ultraviolet light shows
remnants of a similar pattern.

PETUCH (1979) placed Cypraea mus and the C. henekeni
complex in Syphocypraea Heilprin, 1887, on the basis of
similar conchological morphology in the bulla stages of C.
mus, C. henekeni, and Cypraea (Syphocypraea) problematica
Heilprin, 1887, the type species of the genus. We place
the members of the C. henekeni complex merely in Cypraea,
not Syphocypraea, on the grounds that members of Syph-
ocypraea possess a spiriform posterior canal and not the
deeply cut posterior notch present within the C. henekenz
complex. Shells of S$. problematica have an elongate, ovoid
shell, whereas those of the C. henekeni complex and C. mus
tend to be more anteroposteriorly compressed, angular in

Figure 3

Cypraea zietsmani. Paratype A shell, 56.8 mm long. Ventral
aspect showing pigmented areas when exposed to ultraviolet light.

W. Liltved & F. G. Le Roux, 1988 Page 403

Figure 4

Cypraea fultoni Sowerby, 1903. Shell, 58.4 mm long. Left, dorsal; middle, ventral; and right, lateral aspects.

shape with an elevated dorsal hump. Based on concho- One paratype of Cypraea zietsmani (Figure 5, in part)
logical similarity, the affinities of the C. henekeni-C. mus shows evidence of having been preyed upon by a mollus-
complex appear to be with species placed in the Cypraea civorous fish. Shells of C. fultont Sowerby, 1903 (Figure
subgenus Barycypraea Schilder, 1927, which include C. 4) and C. broderipu Sowerby, 1832 (Figure 5, in part),
fultoni, C. teuleri, and C. zietsmani, rather than with Syph- which are occasionally taken from stomachs of the mus-
ocypraea. selcracker, Cymatoceps nasutus (Castelnau, 1861), caught

Figure 5

Left (dorsal) and middle (ventral): Cypraea zietsmani, paratype E, 59.8 mm long, showing perforations caused by
fish predation. Right, lateral: Cypraea broderipu Sowerby, 1832, 74.1 mm long, showing partially healed perforations
due to predation by Cymatoceps nasutus (Castelnau, 1861).

Page 404

CAPE TOWN @

The Veliger, Vol. 30, No. 4

ANGE OF C. FULTONI

Figure 6

Index map showing areal extent of Alexandria Formation and its possible correlatives—the De Hoopvlei and Uloa
formations. The range of Cypraea fultoni Sowerby, 1903, is shown by the shaded area. The area enclosed within

the rectangle is shown in detail in Figure 7.

in deep water off Natal, occasionally bear round or ovoid
perforations punched out by the powerful, toothed jaws.
The holes are similar to those on the base and dorsum of
paratype E. The interior of paratype F indicates that after
death, the shell became the habitat of a bryozoan colony.
The characteristically bored holes on the base of paratype
H indicate that the shell became riddled by a clionid sponge
afer death.

Etymology: The new species is named for Ross Zietsman
of Port Elizabeth, South Africa, who collected the holotype
and provided some of the type material used in this study.

PALEOECOLOGY

The Alexandria Formation represents a marine deposit of
Neogene age. It unconformably overlies the Mesozoic
Uitenhage Group or the Paleozoic Cape Supergroup as a
veneer on a well-planed, dissected, and stepped seaward-
sloping platform. Discontinuous outcrops of the formation
occupy a narrow strip 20 to 40 km wide, between the
Elands and Suur mountains in the south and the sea. The
westernmost outcroup of the Alexandria formation is
marked by an erosional cut-off in the vicinity of the Gam-
toos River, while the eastern boundary is defined by the
Kowie River (Figure 7). The northern limit of the for-
mation roughly coincides with the 300-m contour, while
southward it may pass below sea level onto the continental
shelf, although it would seem more probable that post-
Tertiary (marine) erosion has removed all but remnants
of the Alexandria Formation in the offshore. The type
area of the formation is situated east of the Sundays River
in the vicinity of Colchester (LE Roux, in press b).

The age of the Alexandria Formation, as indicated by
molluscan as well as foraminiferal assemblages, is Neogene
(SIESSER & DINGLE, 1981), with stratification generally
becoming more recent seawardly.

The formation consists essentially of alternating beds of
whitish gray, fine to medium-grained, calcareous sand-
stone, subordinate shelly conglomerate and coquinite that
contain rich assemblages of marine invertebrates (LE ROUX,
in press a). The formation is normally between 3 and 9
m thick. Sedimentary structures, corroborated by biogenic
structures, fossil assemblages, and the physical condition
of the shells, point to depositional environments ranging
from shoreface and foreshore to lagoonal and/or estuarine.

The Alexandria Formation is correlated with the De
Hoopvlei and Uloa formations (both Neogene) in the
southwestern Cape Province and Natal (LE Roux, in press
b), chiefly owing to lithological, paleontological and chro-
nostratigraphical similarities (Figure 6).

Distribution and inferred habitat: Shells of Cypraea
zietsmani were found at five localities on the lowest of
three terraces. This terrace is tentatively regarded as being
of Pliocene age.

(a) Aloes Siding (44 m elevation) northeast of Port Eliz-
abeth (33°48'56"S, 25°37'49”E). At the type locality, spec-
imens of Cypraea zietsmani were found in a trench, which
has since been closed. The depositional environment, as
inferred from outcrops in the immediate vicinity, is that
of a beach. The locality is situated on one of a number of
beach ridges that parallel the present-day shoreline. These
beach ridges are taken to represent paleo-shorelines of a
regressing sea during the Pliocene. Fossils at this locality

W. Liltved & F. G. Le Roux, 1988

| ALEXANDRIA FORMATION

SUURBERGE

EASTERN CAPE PROVINCE

Page 405

NOGNO?1 1Sv4i XZ:

Figure 7

Distribution of Alexandria Formation (most of the formation is unexposed) (after LE Roux, in press b).

are rare owing to poor exposures, but shells of +Glycymeris
borgest (Cox, 1946), + Melapium patersonae Newton, 1913,
Marginella sp., and Conus sp. were found on the surface.

(b) St. George’s Strand (39 m elevation) northeast of
Port Elizabeth, 33°49'22”S, 25°39'12”E). A foreshore
(beach) depositional environment is inferred for the se-
quence exposed at this locality. Thin pebble-cobble beds
alternate with coquina layers. A thin semiconsolidated
sandstone bed yielded several in sttu Bullia digitalis (Dill-
wyn, 1817) which are typical of a sandy beach environ-
ment. Fossils at this locality include the following (+ =
extinct taxa).

Inferred habitat preference

Gastropoda
Amalda optima (Sow-
erby, 1892)
Amalda obtusa
(Swainson, 1825)
Bullia digitalis (Dill-
wyn, 1817)

subtidal sand
subtidal sand

intertidal sandy beach

Turritella carinifera
Lamarck, 1822

+Vasum sp. nov. ?

Bivalvia

Crassatina capensis
(Lamy, 1917)

+Glycymeris borgesi
(Cox, 1946)

+ Notocallista schwar-
zi (Newton, 1913)

Perna perna (Linné, intertidal/subtidal, rocky
1758) shore

intertidal/subtidal reef
subtidal reef
subtidal sand
subtidal sand

subtidal sand

(c) Coega (60 m elevation) northeast of Port Elizabeth
(33°45'04"S, 25°40'06"E). Two Cypraea zietsmani speci-
mens were found in a coquinite layer that had been de-
posited as a beach berm. The high wave energy that existed
during the deposition of this shelly layer is suggested by
the fragmented and worn nature of the fossil shells. Both
specimens are worn and filled with comminuted shell frag-
ments. Other fossils from this coquinite are the following.

Conus sp.

Fusinus ocelliferus
(Lamarck, 1816)
Heliacus cf. trochoides
(Deshayes, 1830)

+Pseudoliva sp.
nov. ?

Suphonaria aspera
Krauss, 1848

Thais capensis (Petit,
1852)

Thais haemostoma
(Linné, 1767)

reef/sand
intertidal /subtidal, reef/sand

intertidal /subtidal, rocky
shore

sand

intertidal rocky shore

low neaptide downwards reef

intertidal /subtidal reef

Gastropoda

Bullia digitalis (Dill-
wyn, 1817)

Siliquaria cf. wilman-
ae (Tomlin, 1918)

Bivalvia

Arca noae (Linné,
1758)

Barbatia foliata
(Forsskal, 1775)

+Cardium edgari
Newton, 1913

Inferred habitat preference

intertidal sandy beach

subtidal rock

subtidal reef
intertidal rocky shore

sand

Page 406

“vu
MOTHERWELL IS.

+++ RAILWAY
@(c) C. ZIETSMAN! LOCALITIES

Figure 8

Localities of Cypraea zietsmani.

Donax serra Dillwyn,
1817

+Glycymeris borgest sand
(Cox, 1946)

intertidal sandy beach

The Veliger, Vol. 30, No. 4

Brachiopoda
Kraussina sp.
Gastropoda
Dendrofissurella scu-
tellum (Gmelin,
1791)
+Calyptraea kilburni
Kensley and Peth-
er, 1986
+Chonella sp. nov. ?
Diodora elevata
(Dunker, 1846)
Fissurellidea aperta
(Sowerby, 1825)
Melapium elatum
(Schubert and
Wagner, 1829)
Nucella squamosa
(Lamarck, 1816)
Turritella sanguinea
Reeve, 1849
+Vasum sp. nov. ?
Bivalvia
Barbatia obliquata
(Gray, 1837)
+Glycymeris borgesi
(Cox, 1946)
G. cf. quekett: (Sow-
erby, 1897)
+Pinctada sp. nov. ?
Scaphopoda
Dentalium sp.

Inferred habitat preference

reef

intertidal rocky shore
reef

sandy reef

subtidal reef

intertidal /subtidal reef

subtidal sand

subtidal reef

subtidal sand
subtidal reef
intertidal rocky shore
subtidal sand
subtidal

subtidal reef

subtidal sand

Isognomon sp.

Ostrea algoensis Sow-
erby, 1871

+Pinctada sp. nov. ?

Scissodesma spengleri
(Linné, 1767)

Anthozoa
Balanophyllia sp.

reef
intertidal /estuarine rock

reef
intertidal /subtidal sand

reef

(e) Trench at Motherwell, 3 km north of Swartkops
(58 m elevation), Port Elizabeth (33°47'50"S, 25°36'22”E).
Two specimens of Cypraea zietsmani were found in a
fossiliferous pebbly coquinite, deposited as a beach berm.
High wave energy during deposition is suggested by the
fragmented nature of the shells. Fossils associated with this
coquinite are the following.

Echinoidea
Echinodiscus sp. lower intertidal to subtidal

sand

(d) Railway cut 1 km north of Swartkops (43 m ele-
vation) Port Elizabeth (33°50'15"S, 25°36'44”E). Cypraea
zietsmani specimens were found in a fossiliferous, semi-
consolidated conglomerate layer showing typical low-angle
beach stratification as well as imbrication. A sandstone
lens in this unit shows herringbone cross-bedding, which
is also suggestive of a beach environment. The generally
good physical condition of shells in this layer suggests only
moderate wave energy during deposition. Fossils associated
with C. zietsmani at this locality are the following.

Gastropoda
Bulla annulata (La-
marck, 1816)
Melapium elatum
(Schubert & Wag-
ner, 1829)
Bivalvia
Ostrea atherstonei
Newton, 1913
Isognomon cf. gaudi-
chaudi (d’Orbigny,
1842)

Inferred habitat preference

subtidal sand

subtidal sand

subtidal reef

intertidal /subtidal reef

W. Liltved & F. G. Le Roux, 1988

ACKNOWLEDGMENTS

We thank Terrence M. Gosliner of the California Acad-
emy of Sciences, San Francisco, and John Pether of the
South African Museum, Cape Town, for giving valuable
comment on this work, Mr. and Mrs. A. K. Ball of Jef-
frey’s Bay, South Africa, for providing photographs of their
specimens of Cypraea zietsmami, and Patricia Dal Poroto
of the California Academy of Sciences for typing the manu-
script. The second author thanks the Chief Director of the
Geological Survey of South Africa for permission to pub-
lish data collected by the Survey.

LITERATURE CITED

Bourbon, M. & P. MAGNIER. 1969. Notes on the Tertiary
fossils at Birbury, Cape Province. Trans. Geol. Soc. S. Afr.
72(3):123-125.

Page 407

INGRAM, W. M. 1947. Fossil and Recent Cypraeidae of the
western regions of the Americas. Bull. Amer. Paleo. 120:1-
83.

INGRAM, W. M. 1948. Fossils Cypraeidae from the Miocene
of Florida and Colombia. Calif. Acad. Sci., 4th Ser., Proc.
6:125-133.

LE Roux, F. G. In press a. Tertiary macrofossils of the Al-
exandria Formation—a supplementary list. Ann. Geol. Surv.
S. Afr. 21.

LE Roux, F.G. Inpressb. Lithostratigraphy of the Alexandria
Formation. Stratigraphic Description and Amendments 1.
South African Committee for Stratigraphy. Handbook 8 (2).

Petucn, E. J. 1979. A new species of Syphocypraea (Gastro-
poda: Cypraeidae) from northern South America with notes
on the genus in the Caribbean. Bull. Mar. Sci. 29(2):216-
225%

SIESSER, W. G. & R. V. DINGLE. 1981. Tertiary sea-level
movements around southern Africa. Jour. Geol. 89:83-96.

The Veliger 30(4):408-411 (April 1, 1988)

THE VELIGER
© CMS, Inc., 1988

Two New Species of Liotiinae (Gastropoda: Turbinidae)

from the Philippine Islands

JAMES H. McLEAN

Los Angeles County Museum of Natural History, 900 Exposition Boulevard,
Los Angeles, California 90007, U.S.A.

Abstract. "wo new gastropods of the turbinid subfamily Liotiinae are described: Bathyliontia glassi
and Pseudoliotina springsteent. Both species have been collected recently in tangle nets off the Philippine

Islands.

INTRODUCTION

A number of new or previously rare species have been
taken in recent years by shell fishermen using tangle nets
in the Philippine Islands, particularly in the Bohol Strait
between Cebu and Bohol. Specimens of the same two new
species in the turbinid subfamily Liotiinae have been re-
ceived from Charles Glass of Santa Barbara, California,
and Jim Springsteen of Melbourne, Australia. Because
these species are now appearing in Philippine collections,
they are described prior to completion of a world-wide
review of the subfamily, for which I have been gathering
materials and examining type specimens in various mu-
seums. Two other species, Liotina peronu (Kiener, 1839)
and Dentarene loculosa (Gould, 1859), also have been taken
by tangle nets in the Bohol Strait but are not treated here.

Much of the material coming from Philippine tangle
net sources comes from either of two localities: off Punta
Engano, Mactan Island, Cebu (10°18’N, 124°01'E) and
off Balicasag Island, S of Panglao, Bohol (9°31'N,
123°40'E). These localities are at opposite ends of the
Bohol Strait and are separated by a distance of approxi-
mately 100 km. Precise locality information for material
from Philippine tangle nets is impossible to obtain, because
the shell fishermen work the entire area and do not provide
detailed localities (Jim Springsteen, personal communi-
cation). The type localities of the two species described
here are given simply as the Bohol Strait. Maximum depth
for the Bohol Strait is indicated as 190 fathoms on U.S.
Hydrographic Chart no. 14429, from which the coordi-
nates cited above were taken. After conversion to metres,
the depth range is therefore approximately 200-350 m for
this material.

Holotypes are deposited in the Los Angeles County
Museum of Natural History (LACM); additional para-

types are deposited in the LACM, the U.S. National Mu-
seum of Natural History, Washington (USNM), and the
Australian Museum, Sydney (AMS). Additional material
in less perfect condition of the first described species has
been recognized in the collections of the USNM and the
Museum National d’ Histoire Naturelle, Paris (MNHN).

Family TURBINIDAE Rafinesque, 1815
Subfamily LIOTIINAE H. & A. Adams, 1854

The subfamily is characterized by a turbiniform profile,
nacreous interior, fine lamellar sculpture, an intritacalx in
most genera, circular aperture, a multispiral operculum
with calcareous beads, and a radula like that of other
turbinid subfamilies.

Although previously treated by some authors as a full
family, the Liotiinae have recently been ranked as a
subfamily of Turbinidae (MCLEAN, 1987).

Genus Bathyliotina Habe, 1961

Type species (original designation): Liotta armata A. Adams,
1861. Recent, Korea Strait.

Bathyliotina species are characterized by a broad um-
bilical opening, a spinose periphery, and greatly thickened
final lip in which the aperture flares to its greatest extent,
followed by deposition of lamellar layers that evenly de-
crease the diameter of the aperture to its final size. Bathy-
hotina is unique among liotiine genera in having the evenly
decreasing lamellar layers forming the final expanded lip.
Liotina Fischer, 1885, Dentarene Iredale, 1929, and Aus-
troliotia Cotton, 1948, differ from Bathyliotina in having a
greatly expanded lip followed by a constriction and then
a secondary inflation to the final lip only slightly larger

J. H. McLean, 1988

Page 409

Explanation of Figures 1 and 2

Figure 1. Bathyliotina glassi sp. nov. Holotype, LACM 2298.
x 3.1.

than the diameter of the body whorl. Other differences are
that Liotina has a broad cord bordering and narrowing the
umbilicus, Dentarene has an umbilical ridge running into
a twisted appendage of the inner lip, and Austroliotia Cot-
ton, 1948, has a broadly open umbilicus not bordered by
a major cord or a twisted ridge.

There are four previously described species of Bathyli-
otina: B. armata (A. Adams, 1861), B. lamellosa (Schepman,
1908), B. schepmani Habe, 1953, and B. nakayasui Habe,
1981. All occur offshore in the central Indo-Pacific.

Bathyliotina glassi McLean, sp. nov.
(Figure 1)

Description: Shell large for genus, depressed turbinate,
yellowish white, maximum diameter 16.0 mm, whorls 4,
periphery marked by pointed upturned spines, about 12
per whorl; aperture oblique, mature lip greatly expanded;
shell surface marked by fine, sharp lamellar growth in-
crements; lamellae sharp, not coalescing; intritacalx not
evident. Protoconch diameter 200 um, suture deeply im-
pressed, first and second whorl rising above protoconch,
third whorl descending, resulting in flat topped profile for
early whorls. Early sculpture marked by strong axial la-
mellae and swellings at suture and periphery, those at

Figure 2. Pseudoliotina springsteeni sp. nov. Holotype, LACM
2300. x5.3.

periphery forming spines in final two whorls. Spines not
sealed anteriorly, lamellae that form spines broadly spaced
at periphery. Spiral sculpture of two nodulose cords be-
tween suture and periphery. Spiral sculpture on base of
one cord near outer edge, an angular cord defining um-
bilicus, and another within umbilicus. Axial sculpture cor-
responding to spines, forming pronounced ribs close to
umbilicus and forming crenulate border on cord defining
umbilicus and cord within umbilicus. Lip descending be-
low suture on final fifth of last whorl, flaring to full extent
of last spine and marked by lamellar increments of de-
creasing breadth until lip reaches its final resting stage.
Aperture circular, nacreous within. Operculum with nu-
merous volutions, bearing sharply projecting beads. Di-
mensions of holotype: height 8.5, maximum diameter 16.0
mm.

Type locality: Bohol Strait, Philippines, 90-180 m (see
Introduction).

Type material: 5 specimens: 4 specimens from Glass &
Foster collection and 1 specimen from Springsteen collec-
tion. Holotype, LACM 2298; 2 paratypes LACM 2299
(height 7.4, diameter 14.5; height 7.0, diameter 13.9 mm);
1 paratype USNM 784761 (height 8.2, diameter 15.0
mm); 1 paratype AMS (height 8.6, diameter 15.0 mm).

Page 410

Referred material: 13 specimens, Glass & Foster collec-
tion. The following dead shells in poor condition: 4 spec-
imens MNHN, Musorstom Expedition II, sta. DG 32,
off N side Mindoro Island, Philippines (13°40’N,
120°54”E), 192-220 m; 4 specimens (plus 2 juveniles)
USNM 278563, Albatross sta. 5262, off Matacot Point,
W side Luzon, Philippines, 208 m; 1 specimen (plus 3
juveniles) USNM 287574, Albatross sta. 5398, off Gi-
gantangan Island, NW side Leyte, Philippines.

Remarks: Bathyliotina glassi is the only member of the
genus having long peripheral spines. It most resembles B.
schepmani Habe, 1953 (name based on “Liotia (Arene)
armata var.” of SCHEPMAN, 1908:35, pl. 3, fig. 1), from
northeastern Borneo, which is smaller, more elevated, has
some intritacalx, has shorter peripheral spines and a basal
cord that is weakly spinose. Bathyliotina glassi is exceeded
in size only by B. nakayasuz HABE (1981:109, figs. 1-3),
which has short peripheral spines and strong clathrate
sculpture.

The holotype has been previously figured without an
identification (GLASS, 1984).

Etymology: The species is named after Charles Glass, of
Santa Barbara, California, former editor of the Conchol-
ogists of America Bulletin.

Genus Pseudoliotina Cossmann, 1925

Type species (original designation): Liotza sensu: Vidal, 1921.
Upper Cretaceous, Europe.

Pseudoliotina species are characterized by an extremely
flat spire, presence of intritacalx, nearly planispiral coiling,
forming an extremely broad umbilicus, and thickened final
lip. The aperture has a terminal constriction that produces
a secondary final lip following the major thickening, sim-
ilar to that noted above for the genera Liotina, Dentarene,
and Austroliotia.

Pseudoliotina has previously been treated (KEEN, 1960)
as a synonym of Cyclostrema Marryat, 1818, but is here
distinguished from that genus. Species of Cyclostrema are
larger than those of Pseudoliotina and do not produce a
thickened final lip. Cyclostrema is restricted to two species
in the Caribbean faunal province: the type species C. can-
cellatum Marryat, 1818, and C. tortuganum Dall, 1927,
both of which were reviewed by ABBOTT (1950).

Only three species have the characters of the aperture
defined above: the fossil type species, the broadly distrib-
uted Indo-Pacific species P. discoidea (Reeve, 1843), and
the following new species.

Pseudoliotina springsteent McLean, sp. nov.
(Figure 2)

Description: Shell large for genus, discoidal, yellowish
white, maximum diameter 10.5 mm, whorls 3.5, periphery

The Veliger, Vol. 30, No. 4

marked by blunt double spines, 12 on final whorl; aperture
only slightly oblique; mature lip thickened; whole surface
of shell with fine, sharp lamellar growth increments, sur-
face choked with intritacalx. Protoconch diameter 200 um,
suture deeply impressed, teleoconch whorls rising above
and below protoconch to maintain discoidal profile, except
on final fifth of whorl preceding lip, where suture descends,
placing final aperture below position of previous whorls.
Discoidal growth results in extremely broad umbilicus,
revealing basal side of early whorls. Final whorl in contact
with penultimate whorl only at tips of spines. Spiral sculp-
ture of single, faint, mid-dorsal carination, and weak, dou-
ble, peripheral cords that produce the tight, double spi-
nation; base with two cords, outermost cord nodose to
correspond to spines; inner cord smooth; umbilical edge
with two crisply crenulate cords; umbilical wall with two
additional, finely fluted cords. Umbilical wall also with
fine spiral threads not apparent on rest of shell. Lip thick-
ened, buttressed behind by swollen spiral cords; final swell-
ing of lip separated from flaring extent of lip by deep pits.
Aperture circular, nacreous within. Operculum unknown.
Dimensions of holotype: height 3.9, maximum diameter
10.5 mm.

Type locality: Bohol Strait, Philippines, 200-350 m (see
Introduction).

Type material: 4 specimens from Springsteen collection.
Holotype, LACM 2300, 1 immature paratype LACM
2301 (height 2.6, diameter 7.6 mm); 1 paratype USNM
784726 (height 4.0, diameter 10.8 mm); 1 paratype AMS
(height 4.3, diameter 10.3 mm).

Referred material: 3 specimens (1 immature) Glass &
Foster collection. No additional material is known; spec-
imens have not been recognized in any museum collections.

Remarks: The sculpture of Pseudoliotina springsteent is
so intricate that no other species is remotely similar. Pseu-
doliotina discoidea (Reeve, 1843) is smaller and has sculp-
ture of spiral cords with no peripheral spines. The type
species also lacks the strong peripheral spines of P. spring-
steent.

Etymology: The name honors Jim Springsteen of Mel-
bourne, Victoria, Australia, author of Shells of the Phil-
ippines (SPRINGSTEEN & LEOBRERA, 1986).

ACKNOWLEDGMENTS

I am grateful to Charles Glass and Robert Foster of Santa
Barbara, California, and Jim Springsteen, of Melbourne,
Victoria, Australia, for loan of material and donation of
type material of the new species. I thank Philippe Bouchet
of the Paris Museum, and Richard Houbrick of the U.S.
National Museum, for the loan of additional material.
Helpful commentary was provided by Carole S. Hickman,
University of California, Berkeley.

J. H. McLean, 1988

LITERATURE CITED

ApBoTT, R. T. 1950. The genus Cyclostrema in the western
Atlantic. Johnsonia 1(27):193-200.

Gass, C. 1984. Mystery shell. Conch. Amer. Bull. 12(1):18,
fig. not numbered.

Hasse, T. 1953. Addenda and corrigenda. Illustrated catalogue
of Japanese shells, no. 25:213-215.

Hasse, T. 1981. A new species of the genus Bathyliotina from
off Formosa, South China Sea. Venus, Jap. Journ. Malacol.
40(2):109-110.

KEEN, A. M. 1960. [Cenozoic Archaeogastropoda]. Jn: R. C.
Moore (ed.), Treatise on invertebrate paleontology, Part I.

Page 411

(Mollusca 1). Geological Society of America and University
of Kansas Press. xi1 + 351 pp.

McLEan, J. H. 1987. Angariinae and Liotiinae—the primitive
living trochaceans. Ann. Rept. Western Soc. Malacol. 19:
16.

SCHEPMAN, M. M. 1908. The Prosobranchia of the Siboga
Expedition. Part 1. Rhipidoglossa and Docoglossa. Resultats
des Explorations Zoologiques, Botaniques, Oceanogra-
phique et Geologique ... a bord du Siboga. Monographie
49a, Livre 39:1-107, 9 pls.

SPRINGSTEEN, F. J. & F. M. LEoBRERA. 1986. Shells of the
Philippines. Carfel: Manila. 377 pp.

The Veliger 30(4):412-416 (April 1, 1988)

THE VELIGER
© CMS, Inc., 1988

Six New Species of Terebridae (Mollusca: Gastropoda)

from Panama and the Indo-West Pacific

TWILA BRATCHER

Los Angeles County Museum of Natural History, Malacology Section, Exposition Park,
Los Angeles, California 90007, U.S.A.

Abstract.

Six new species of Terebridae are described: Terebra rancheria, Isla Rancheria, Gulf of

Chiriqui, Panama; 7. paucincisa, Granc Récif South, New Caledonia; 7. albocancellata, Chesterfield-
Bellona Plateau, Coral Sea; 7. macleam, East Cape, East London, South Africa; Hastula alboflava,
Sogod,.Cebu, Philippine Islands; and H. colorata, Lighthouse Beach, Western Australia.

Six new species of Terebridae have come to my attention
too late to be included in the book Living Terebras of the
World (BRATCHER & CERNOHORSKY, 1986). To date 267
valid species have been described in the Terebridae, which
has world-wide tropical and temperate zone distribution,
with the majority of species living in the warmer waters
of the tropics. They live in sand or sandy mud from the
intertidal zone to a depth of about 1000 m.

It has been 15 yr since a new Panamic terebrid has been
described. In 1986 Carol Skoglund brought to my attention
one dredged off Isla Rancheria, a small islet near the large
Coiba Island, which houses Panama’s penal colony. Since
then additional lots have been dredged in the same general
area.

Seven lots of a new species of 7erebra were among ma-
terial collected by 250 dredge hauls made in New Cale-
donia. This material was sent for identification by Dr.
Philippe Bouchet of the Museum National d’ Histoire Na-
turelle of Paris. Shortly after noting the new species, I
received additional specimens of the same species collected
in Fiji by Brian Parkinson.

Along with the New Caledonian material sent by Dr.
Bouchet were some lots from the Chesterfield Islands, be-
tween New Caledonia and Queensland. These contained
two lots of another new species.

Dr. Richard Kilburn of the Natal Museum in South
Africa sent another new species dredged from the Agulhas
Bank, an area that contains predominately endemic mol-
lusks.

For the past 15 yr I have had specimens of an unusually
shiny undescribed species of Hastula that are colored in clear
pastels of pink, peach, lavender, yellow, and white. I have

postponed describing the species until I could see a live-
collected specimen or at least a good beach specimen. The
species appears to be endemic to southwestern Australia.
Both the Australian Museum at Sydney and the Western
Australian Museum at Perth had many specimens of this
species, but all were damaged. On a recent trip to Western
Australia I failed to find anyone who had collected this
species alive, but Wendy Anson kindly gave me some beach
specimens in fine condition, of which the holotype is part.
Another new species of Hastula was brought to my at-
tention by the Philippine collector Fernando Dayrit.

ABBREVIATIONS

Abbreviations have been used for a number of institutional
collections cited in this paper, as follows.

AMNH—American Museum of Natural History, New
York

AMS—Australian Museum, Sydney

ANSP—Academy of Natural Sciences of Philadelphia

BM(NH)—British Museum (Natural History), London

CAS—California Academy of Sciences, San Francisco

LACM—Los Angeles County Museum of Natural His-
tory

MCZ—Museum of Comparative Zoology, Harvard Uni-
versity, Cambridge

MORG—Museu Oceanografico de Rio Grande, Brazil

NM—Natal Museum, South Africa

SDMNH-—San Diego Museum of Natural History, San
Diego

WAM—Western Australian Museum, Perth

T. Bratcher, 1988

TEREBRIDAE Morch, 1852
Terebra Bruguiere, 1789
Terebra rancheria Bratcher, sp. nov.
(Figures 6, 8)

Diagnosis: Small (maximum length 17 mm) Tevebra with
purplish black below the periphery of the body whorl,
including the columella and siphonal fasciole.

Description: Shell small for the genus with 11 whorls of
the teleoconch; protoconch of 1.5 pale mamillate whorls;
outline of whorls almost straight; subsutural band flat,
marked by deep punctations between ribs; axial ribs curved,
indistinct, narrower than interspaces, 27 on penultimate
whorl; spiral grooves weak, not crossing ribs, 4 rows on
penultimate whorl; body whorl with broken spiral grooves
coalescing into continuous grooves at periphery; aperture
semi-elongate; columella straight; color grayish white with
a few early whorls of dark amber and area beginning
anterior to periphery of body whorl dark purple, including
columella and siphonal fasciole.

Dimensions: Holotype 16.9 x 4.0 mm; paratypes from
12.5 x 3.1 mm to 15.6 xX 3.4 mm.

Type locality: Off Isla Rancheria, Gulf of Chiriqui, Pan-
ama (7°38’N, 81°44'W), 3.5 m, white sand bottom with
some broken shell.

Type material: Holotype LACM 2261; paratypes AMNH
222586 (1); ANSP (1); BM(NH) 1986259 (1); CA S(1);
MORG 24.808 (1); SDMNH 29522 (1); USNM 859147
(1); Bratcher coll. (4); Koch coll. (4); Skoglund coll. (10).

Discussion: On most species of Zerebra with dark stains
on the anterior of the shell, the stain begins at the periphery
of the body whorl. The stain on this species begins anterior
to the periphery. Of the 26 specimens, the only variation
is that several are slightly darker with lighter subsutural
bands, and one lacks the dark purple anterior. It has a
light brownish stain in that area.

The only species with which Terebra rancheria can be
compared is 7. churea Campbell, 1964, from which it
differs by having a flatter outline, flatter subsutural band,
fewer spiral grooves, and a blackish-purple anterior.

The name of the species is derived from Isla Rancheria,
the type locality.

Terebra paucincisa Bratcher, sp. nov.
(Figure 4)

Diagnosis: A moderately small (maximum length 24 mm)
Terebra with features somewhat resembling 7. nitida Hinds,
1844, and Duplicata raphanula (Lamarck, 1822) with oc-
casional spiral grooves and a paucispiral protoconch.

Description: Shell moderately small, slender, with 12 shiny
whorls of the teleoconch; protoconch of 1.5 bulbous trans-

Page 413

lucent whorls; outline of whorls slightly curved; subsutural
band beginning on 4th whorl, defined by deep punctations
between ribs; axial ribs narrower than interspaces, un-
broken from suture to suture on early whorls and later
becoming thickened slightly on subsutural band; spiral
sculpture of occasional faint grooves between some ribs, 2
on penultimate whorl; body whorl with axial ribs becoming
almost obsolete on final one-half of whorl; aperture elon-
gate; columella with heavy parietal callus and with narrow
brown line on inner edge; siphonal fasciole with sharp
keel; color warm beige with brown nebulous streaks and
a narrow light stripe on periphery of body whorl visible
through aperture.

Dimensions: Holotype 19.7 x 4.0 mm; paratypes from
19.1 x 3.8 mm to 23.9 x 4.8 mm.

Type locality: Grand Recif South, New Caledonia,
22°37'S, 166°51’'E, 17 m.

Type material: Holotype and 12 paratypes MNHNP;
other paratypes AMNH 222587 (1); AMS C15234 (1);
BM(NH) 1986260 (1); CAS (1); LACM 2260 (1); MCZ
296165 (1); USNM 859148 (1); Bratcher coll. (9); Par-
kinson coll. (6); Cernohorsky coll. (2).

Distribution: New Caledonia to Fiji and the Philippine
Islands.

Discussion: The color varies from almost black to cream
with a few darker or brownish blotches. Two individuals
from Fiji and two from New Caledonia are grayish white
with few brownish blotches and with the edge of the si-
phonal fasciole and inner lip outlined in gold. Many of
the light-colored shells have a dark blotch on the dorsum
of the body whorl. Most of the black specimens were found
living in black volcanic sand in Fiji. The color of the
protoconch varies from blackish brown on the holotype to
translucent cream, some with an opaque dark stripe with-
in. The axial ribs become more obsolete on some specimens
than on others. The grooves are usually discontinuous,
often very short and faint or almost missing.

This species bears some resemblance to both Jerebra
nitida and Duplicaria raphanula, both of which have larger
shells with slender multi-whorled protoconchs in contrast
to the short bulbous protoconch of this species. In addition,
D. raphanula may be separated from this species by its”
more irregular axial ribs, which sometimes fade below the
subsutural band. Terebra nitida has more widely spaced
ribs than this species.

The name is derived from the Latin paucus, meaning
“few,” and incise, meaning “cut into.”

Terebra albocancellata Bratcher, sp. nov.

(Figures 1, 9)

Diagnosis: A slender, dull-white Indo-Pacific 7erebra with
cancellate sculpture, small for the genus, maximum length
18.8 mm.

Page 414 The Veliger, Vol. 30, No. 4

T. Bratcher, 1988

Description: A slender, small Terebra with teleoconch of
12 whorls; protoconch of 3.5 conical whorls; outline of
whorls straight; subsutural band defined by groove cutting
through riblets; axial riblets fine, narrow, numerous, slant-
ing to right on subsutural band, curving to left on re-
mainder of whorl, 34 on penultimate whorl; spiral threads,
5 on penultimate whorl, crossing riblets to form cancellate
sculpture with small pustules forming at intersections; body
whorl with cancellate sculpture continuing to siphonal
fasciole; aperture semi-elongate; columella with heavy pa-
rietal callus; color dull white.

Dimensions: Holotype 18.8 x 3.4 mm; paratypes from
14.8 x 3.4 mm to 15.0 x 3.8 mm.

Type locality: Plateau Chesterfield-Bellona Chalcal, Cor-
al Sea, 36°42’S, 158°59’E.

Type material: Holotype and 1 paratype MNHNP; 1
paratype Bratcher coll.

Distribution: Chesterfield Islands, Coral Sea (between
New Caledonia and Queensland, Australia).

Discussion: Three specimens were dredged from two lo-
calities in the Chesterfield Islands. These show almost no
variation. There is no other small white cancellate Indo-
Pacific species with which this could be confused. An im-
mature specimen of Terebra conspersa Hinds, 1844, bears
a slight superficial resemblance, but does not have the
spiral grooves crossing the axial ribs, and it does not have
a parietal callus. Also 7. conspersa is a warm beige with
a few tiny brown dots and with a brownish stain anterior
to the periphery of the body whorl in contrast to the white
of 7. albocancellata.

The name for this species is from the Latin albus, mean-
ing “white,” and cancellatus, meaning “‘lattice-like.”

Terebra macleami Bratcher, sp. nov.
(Figures 3, 10)

Diagnosis: A moderately small 7evebra with no subsutural
band and sculpture of axial striae only.

Description: Shell of medium size for the genus (maxi-
mum length 22.8 mm) with no subsutural band and sculp-
ture of axial striae only.

Page 415

Description: Shell of moderate size for the genus with 9
dull-surfaced whorls of teleoconch; protoconch of 1.5 large
mamillate pale amber whorls. Outline of whorls slightly
convex; suture well marked; no subsutural band; axial
sculpture of very fine crowded striae running from suture
to suture; no spiral sculpture; body whorl elongate with
axial striae unbroken from suture to siphonal fasciole;
aperture quadrate; columella almost straight; operculum
yellowish amber; color dull amber.

Dimensions: Holotype 22.8 x 5.1 mm; paratype 21.9 x
5.2 mm.

Type locality: E. Cape of East London, South Africa,
33°04.9'S, 27°54.0'E, muddy sand with lumps of black
mud.

Type material: Holotype NM D473/3687; 1 paratype
NM D4809/T3688.

Distribution: This species is known only from the type
locality.

Discussion: Compared to this species, 7erebra albida Gray,
1834, has a more inflated body whorl and a very weakly
indicated subsutural groove. Also, the range appears to be
confined to Victoria and Western Australia.

This species is named in honor of Dr. James McLean
for his contributions to malacology.

Hastula alboflava Bratcher, sp. nov.
(Figures 2, 5)

Diagnosis: A yellow Hastula of moderate size for the genus
(maximum length 27.3 mm) with a white subsutural band
marked by color rather than sculpture and with ribs below
the suture fading anteriorly.

Description: Shell of moderate size for the genus with 13
shiny whorls of teleoconch; protoconch of 1.25 bulbous
whorls; outline of whorls straight; subsutural band defined
only by a white band, no subsutural groove or punctations;
axial ribs about equal to interspaces, running from suture
to suture on early whorls, fading anteriorly on later whorls;
no spiral sculpture; body whorl with ribs becoming obsolete
below white subsutural band; aperture elongate; siphonal
fasciole exceptionally large for size of shell; color golden
yellow with white band below suture.

Explanation of Figures 1 to 10

Figure 1. Terebra albocancellata sp. nov., holotype, 18.8 x 3.4
mm.

Figure 2. Hastula alboflava, holotype, 24.8 x 4.9 mm.
Figure 3. Terebra macleami, holotype 22.8 =< 5.1 mm.
Figure 4. Terebra paucincisa, holotype 19.9 x 4.0 mm.

Figure 5. Same shell as Figure 2, close-up of middle whorls.

Figure 6. Same shell as Figure 8, close-up of middle whorls.
Figure 7. Hastula colorata, holotype, 14.9 x 4.3 mm.
Figure 8. Terebra rancheria, holotype, 16.9 x 4.0 mm.
Figure 9. Same shell as Figure 1, close-up of middle whorls.

Figure 10. Same shell as Figure 3, close-up of middle whorls.

Page 416

Dimensions: Holotype 24.8 <x 4.9 mm; Paratypes from
16.3 x 3.4 mm to 27.3 X 5.4 mm.

Type locality: Off Sogod, Cebu, Philippine Islands, 15.5

m.

Type material: Holotype LACM 2262; paratypes AMNH
222588 (1); AMS C15235 (1); ANSP (1); BM(NH)
1986261 (1); CAS (1); MCZ 196166 (1); MORG 24.809
(1); NM 758/13690 (1); MNHNP (1); SDMNH 92523
(1); USNM 859149 (1); Bratcher coll. (4); Cernohorsky
coll. (1); Dayrit coll. (41); Marquet coll. (1).

Distribution: Cebu, Philippine Islands.

Discussion: This species bears a resemblance to Hastula
albula (Menke, 1843), which has a protoconch of 4.5 often
blackish-purple conical whorls. The protoconch of H. al-
boflava has 1.25 bulbous whorls. Hastula albula is variable
in color, usually in the same lot, while all 59 examined
specimens of H. alboflava are golden yellow with a white
subsutural band. Except for minimal differences in size,
there is almost no intraspecific variation in the specimens
examined.

The name of this species is from the Latin albus, meaning
“white,” and flavus, meaning “golden yellow,” the colors
of the shell.

Hastula colorata Bratcher, sp. nov.
(Figure 7)

Diagnosis: A shiny, small, bright pastel or white Hastula
with no visible sculpture.

Description: Shell with glassy shine, 9 whorls in teleo-
conch; protoconch of 1.25 short bulbous, bright pink whorls,
larger than following whorls; outline of whorls straight;
no subsutural band or groove; no axial sculpture except
for faint striae under extreme magnification; no spiral
sculpture; body whorl with no sculpture; aperture quad-
rate; columella straight; color bright pink.

Dimensions: Holotype 14.9 x 4.3 mm; paratypes from
11.1 x 2.9 mm to 19.6 x 4.6 mm.

Type locality: Light House Beach, Augusta, Western
Australia, 34°20’S, 115°10’E, beach.

Type material: Holotype WAM 514-86 (pink); paratypes
AMNH 222984 (1 light pink); AMS C153006 (1 white);
ANSP (1 lavender); BM(NH) 1986283 (1 pink); CAS (1
white); LACM 2263 (1 pink); MCZ 296167 (1 pale pink);
MORG 24.810 (1 pale lavender); NM K175/T3689 (1
pale pink); SDMNH 92524 (1 light peach); USNM

The Veliger, Vol. 30, No. 4

859218 (1 purple); Anson coll. (2); Bratcher coll. (4);
Buick coll. (1); Cernohorsky coll. (1); Marrow coll. (4).

Distribution: Southwest Australia.

Discussion: This is the only Hastula species that has been
found in so many clear pastel colors: white, yellow, peach,
rose lavender, and purple, all monochromatic. All 14 type
specimens and many others examined in museums were
beach specimens. As far as is known, no one has collected
a live specimen.

This species differs from Terebra albida by being shiny,
smaller, more slender, and by lacking the inflated body
whorl. It also lacks the indication of a subsutural band
found on H. albida. Hastula colorata does not resemble
juvenile H. albida (W. Anson, personal communication).

The name is from the Latin coloratus, meaning “color
or tinge,” because of the many colors in which the species
is found.

ACKNOWLEDGMENTS

I am greatly indebted to Wendy Anson, Donald Dan,
Fernando Dayrit, Brian Parkinson, Carol and Paul Skog-
lund, and Thora Whitehead for the contribution of para-
types. I thank Dr. Philippe Bouchet, Museum National
d’Histoire Naturelle, Paris, Dr. Richard Kilburn, Natal
Museum, Jan Loch, Australian Museum, and Dr. Fred
Wells, Western Australian Museum, for the loan of ma-
terial from their institutions. Also for the loan of material
for study I thank W. Buick and Max Marrow of Australia,
Robert Koch of Arizona, and Jose Marquet of Belgium.
I add my appreciation to Dr. James McLean for the critical
reading of the manuscript.

LITERATURE CITED

BRATCHER, T. & W. CERNOHORSKY. 1986. Living terebras of
the world. American Malacologists, Inc.: Melbourne, Flor-
ida. 24 pp., 74 pls.

CAMPBELL, G. B. 1964. New terebrid species from the eastern
Pacific (Mollusca: Gastropoda). Veliger 5(3):101-103.
Gray, J. E. 1834. Enumeration of the species of the genus

Terebra. Proc. Zool. Soc. Lond. Pt. 2:59-63.

HInps, R. B. 1844. Description of new shells, collected during
the voyage of the Sulphur, and in Mr. Cuming’s late visit
to the Philippines. Proc. Zool. Soc. Lond. (1843) Pt. 11:
149-168.

LaAMARCK, J. B. P. A. DE M. 1822. Histoire naturelle des
animaux sans vertebres. Mollusques. Paris. 7:1-711 (Tere-
bra, pp. 283-291).

MENKE, C. T. 1843. Molluscorum Novae Hollandiae. A. Hahn:
Hanover. 46 pp.

The Veliger 30(4):417-420 (April 1, 1988)

THE VELIGER
© CMS, Inc., 1988

Assignment to Genus Naesiotus (Albers, 1850) of

Several Species Formerly Assigned to
Rabdotus (Albers, 1850)

(Gastropoda: Pulmonata: Bulimulidae)

JAMES E. HOFFMAN

Department of Ecology & Evolutionary Biology, University of Arizona,
Tucson, Arizona 85721, U.S.A.

Abstract.

The following species formerly assigned to Rabdotus are assigned to the genus Naesiotus

on the basis of anatomical and conchological evidence: Rabdotus nigromontanus (Dall, 1897); R. chris-
tensent Miller & Reeder, 1984; R. milleri Hoffman, 1987, of southern Arizona and Sonora, Mexico;
and R. pallidior (Sowerby, 1833); R. riumatus (Pfeiffer, 1846); R. excelsus (Gould, 1853); R. xantusi
(Binney, 1861); R. spirifer (Gabb, 1868); R. gabbi (Crosse and Fischer, 1872); R. belding: (Cooper,
1892); R. altus (Dall, 1893); R. montezuma (Dall, 1893); R. veseyranus (Dall, 1893); R. cosmicus (Mabille,
1895); R. dentifer (Mabille, 1895); R. ceralboensis (Hanna, 1923); R. chamberlini (Hanna, 1923); R.
hanna (Pilsbry, 1927); R. gigantensis Christensen & Miller, 1977; and R. laevapex Christensen &

Miller, 1977, from Baja California, Mexico.

While working on the zoogeography and interrelationships
of several land snail species that had been placed in the
genus Rabdotus Albers, 1850, I found that some of them
more closely matched the diagnosis of Naesiotus Albers,
1850, according to BREURE (1979). These species were
from southern Arizona, and from Sonora and Sinaloa,
Mexico. I also found that a number of species from Baja
California, Mexico, seemed, from drawings of their re-
productive anatomy (CHRISTENSEN, 1978), to be in the
genus Naesiotus.

The diagnostic points of difference between Rabdotus
and Naesvotus lie in the reproductive anatomy and embry-
onic whorls of the shell. In the reproductive tract of Rab-
dotus, the vagina and penis are typically short (Figure 1),
the glandular part of the penis consists largely of “‘pouches”’
(BREURE, 1979), and the spermathecal duct becomes broad
midway along its length and has ridges within its lumen
(CHRISTENSEN, 1978; Hoffman, unpublished data). In the
reproductive tract of Naesiotus, the vagina and penis are
typically longer (Figure 1), the glandular portion of the
penis consists largely of tubules, and the spermathecal duct
is uniformly narrow and cylindrical, lacking internal ridges
(HOFFMAN, 1987; BREURE, 1979; BREURE & COPPOIS,

1978; CHRISTENSEN, 1978). The embryonic whorls of the
shells of both genera have axial riblets, but the embryonic
whorls of Naesiotus have very fine spiral threads in the
interstices between the riblets, while Rabdotus lacks them
(BREURE, 1979; BREURE & Coppols, 1978) (Figure 2).
While trying to deduce the relationships and geograph-
ical source of a complex of snails including Rabdotus mi-
gromontanus (Dall, 1897), R. christenseni Miller & Reeder,
1984, and R. miller’ Hoffman, 1987, I concluded that they
had all of the characteristics of Naesiotus. By comparing
reproductive anatomies and apical sculptures of other bu-
limulid snails that occur in northern Mexico and the south-
western United States, I found that all, with the exception
of some of those in Baja California, were of the Rabdotus
type. Within Baja California, snails listed by CHRISTENSEN
(1978) as subgenus Leptobyrsus have, in the cases when
they were obtainable, reproductive anatomies typical of
Naesvotus. In most cases the embryonic sculptures also con-
tained the spiral threads (Table 1). I, therefore, place the
three species mentioned above as well as those in Table 1
in the genus Naesiotus. I was unable to obtain either the
reproductive anatomy or shells of R. ceralboensis (Hanna,
1923); R. chamberlini (Hanna, 1923) lacks all shell sculp-

Page 418

Figure 1

A. Genitalia of Rabdotus bailey: (Dall, 1893), J. E. Hoffman
Collection No. 54A. B. Genitalia of Naesiotus nigromontanus, J.
E. Hoffman Collection No. 52A: EC, epiphallic cecum; EP,
epiphallus; PE, penis; SD, spermathecal duct.

ture, and its reproductive anatomy was also unavailable.
However, because of traits that the latter two species have
in common with other snails that Christensen placed in
Leptobyrsus, I tentatively place them in Naesiotus. Species
listed by CHRISTENSEN (1978) as belonging to subgenera

The Veliger, Vol. 30, No. 4

\ As C

\ WAN NS

AWS SS

Figure 2

A. Apex of the shell of Rabdotus bailey: from Sonora, Mexico, J.
E. Hoffman Collection No. 10. B. Apex of the shell of Naesiotus
christenseni from Arizona, W. B. Miller Collection No. 7216. C.
Apex of the shell of Naesiotus tanner: from Isla. Sta. Cruz, Ec-
uador, J. E. Hoffman Collection No. 250.

Plicolumna and Rabdotus s.s., on the other hand, have typ-
ical Rabdotus characteristics.

Previously, Naestotus was thought to be limited to South
America, with its northern limit in Ecuador. These changes
in assignment, of course, greatly increase the range of
Naesiotus and indicate that the genus has a disjunct dis-

J. E. Hoffman, 1988 Page 419

dw

eet
ri

Figure 3

Proposed distribution of the genus Naesiotus.

tribution (Figure 3). Disjunct distributions are not rare,
either among the Bulimulidae or land snails in general.
In fact the “new” distribution of Naesiotus almost matches
the disjunct distribution of Bulimulus Leach, 1815, a closely
related genus, as well as that of the two subfamilies of
Helminthoglyptidae: the Helminthoglyptinae of western

North America and the Epiphragmaphorinae of western
South America. Possible explanations for this disjunct pat-
tern might be that snails near the center of a large range
have died out, or plate tectonics may have been involved.
The alternative possibility of convergent evolution seems
unlikely because of the diverse nature of the traits involved.

Page 420

Table 1

Reproductive traits and embryonic sculpture in Baja Cal-
ifornia snails assigned to the genus Naeszotus.

Embryonic Sculpture Naesiotus type

Species riblets threads repro. anatomy

gigantensis Christensen

& Miller, 1977 yes yes not available
dentifer (Mabille,

1895) yes yes not available
gabbi (Crosse & Fi-

scher, 1872) yes yes yes
hanna (Pilsbry, 1927) yes yes yes
spirifer (Gabb, 1868) shell unavail. yes
rimatus (Pfeiffer, 1846) yes yes yes
veseyianus (Dall, 1893) shell unavail. yes
excelsus (Gould, 1853) yes no* yes
pallidior (Sowerby,

1833) yes yes yes
harribaueri (Jacobson,

1958) yes no yes
cosmicus (Mabille,

1895) yes yes yes
montezuma (Dall,

1893) yes no yes
belding: (Cooper, 1892) yes yes yes
altus (Dall, 1893) shell unavail. probably
laevapex Christensen &

Miller, 1977 no no yes
xantust (Binney, 1861) yes yes yes

* Threads may have been missed owing to very weak embryonic
sculpture in this species.

The Veliger, Vol. 30, No. 4

ACKNOWLEDGMENTS

I am deeply indebted to Walter B. Miller for the loan for
his specimens, especially those from Baja California, Mex-
ico, and for much helpful discussion and advice. In addi-
tion, I wish to thank Robert Van Syoc and the California
Academy of Sciences for the loan of specimens of Naesiotus
from the Galapagos Islands.

LITERATURE CITED

BREURE, A. S. H. 1979. Systematics, phylogeny and zooge-
ography of Bulimulinae (Mollusca). Zool. Verh. Leiden 168:
1-215.

BREuRE, A. S. H. & G. Coppois. 1978. Notes on the genus
Naesiotus Albers, 1850 (Mollusca, Gastropoda, Bulimuli-
dae). Neth. Jour. Zool. 28(2):161-192.

CHRISTENSEN, C. C. 1978. A revision of the genus Rabdotus
(Pulmonata: Bulimulidae) in Baja California, Mexico. Ph.D.
Dissertation, E9791, Univ. of Arizona, Tucson, Arizona. i-
xiv + 354 pp.

HOFFMAN, J. E. 1987. A new species of Rabdotus (Gastropoda:
Pulmonata: Bulimulidae) from Sonora, with a description
of the reproductive anatomy of Rabdotus nigromontanus. Ve-
liger 29:419-423.

MILLER, W. B. & R. L. REEDER. 1984. A new species of
Rabdotus (Gastropoda: Pulmonata: Bulimulidae) from Ari-
zona. Bull. S. Calif. Acad. Sci. 83(2):106-109.

The Veliger 30(4):421-426 (April 1, 1988)

THE VELIGER
© CMS, Inc., 1988

NOTES, INFORMATION & NEWS

Mexichromis tura: Range Extension of a
Rarely Observed Nudibranch
by
Alex Kerstitch
10700 E. Calle Vaqueros,
Tucson, Arizona 85749, U.S.A.
and
Hans Bertsch
Biological Sciences, National University,
8 Executive Circle,
Irvine, California 92714, U.S.A.

Only nine specimens of the Chromodorididae species Mex-
ichromis tura (Marcus & Marcus, 1967) have been re-
corded. The holotype specimen was collected at Deale
Beach, Ft. Kobbe Beach, Panama (8°48’N, 79°55'’W),.
BERTSCH et al. (1973) reported four specimens from Sa-
yulita, Nayarit, Mexico (21°15’N, 105°15’'W). BERTSCH
(1978) cited three specimens from La Cruz, Nayarit
(21°30'N, 105°16’W) and one specimen from La Paz, Baja
California Sur (24°11'N, 110°23’W).

Because of the apparent rarity of this species in collec-
tions, our greater than 400 km northward range extension
is noteworthy. On 24 June 1987, four specimens (one
measuring 12 mm long) of Mexichromis tura were observed
by A. Kerstitch at Bahia San Carlos, Sonora, Mexico
(27°55'N, 111°904’W), in 20 m depth. These specimens
represent the first collection of this species in the eastern

Figure 1

Mexichromis tura collected at San Carlos; photo by Alex Kerstitch.

and central Gulf of California and from the shores of
Sonora.

The mantle margin of the animal illustrated (Figure 1)
was rimmed with three encircling bands: an outermost
yellow, a middle black, and an innermost powder blue.
The black dorsum had numerous yellow spots; the pe-
riphery of the dorsum had larger, whitish streaks and
splashes. The gills were white, with black tips. The rhi-
nophores were completely black.

Literature Cited

BertscH, H. 1978. The Chromodoridinae nudibranchs from
the Pacific coast of America.—Part III. The genera Chro-
molaichma and Mexichromis. Veliger 21(1):70-86.

BerTSCcH, H., A. J. FERREIRA, W. M. FARMER & T. L. HAYEs.
1973. The genera Chromodoris and Felimida (Nudibranchia:
Chromodorididae) in tropical west America: distributional
data, description of a new species, and scanning electron
microscopic studies of radulae. Veliger 15(4):287-294.

Marcus, Ev. DU BoIs-REYMOND & ER. Marcus. 1967. Amer-
ican opisthobranch mollusks. Stud. Trop. Ocean. (Univ.
Miami Inst. Mar. Sci., Miami, Florida), No. 6:vili + 256

PP-

New Record of the Coral Clam
Coralliophaga coralliophaga (Gmelin, 1791)
(Bivalvia: Trapezidae) in the
Mediterranean Sea
by
Carmen Salas
Dept. Zoologia, Facultad de Ciencias,
Universidad de Malaga, 29071-Malaga, Spain
Agustin Barrajon
C/Nuzas, BI. 7-5°-A, 29010-Malaga, Spain
and
Francisco Carpena
C/Nuzas, Bl. 7-6°A, 29010-Malaga, Spain

The family Trapezidae Lamy, 1920, contains three living
genera, species of which live on coral bottoms: 7rapezium
Miuhlfeld, 1811, distributed along Madagascar, the Indo-
Pacific and Japan; Coralliophaga Blainville, 1824, which
is present in the Mediterranean, Atlantic and Indo-Pacific;
and Isorropodon Sturany, 1854, from the deep sea in the
eastern Mediterranean (FRANC, 1960).

Up to now, only two species of this family have been
recorded in the Mediterranean (PIANI, 1980): Corallio-
phaga lithophagella (Lamarck, 1819), a species with a wide
geographical distribution—Atlantic (Britain to Senegal and
the Azores) and Mediterranean (NORDSIECK, 1969)—and
Isorropodon perplexum (Lamarck, 1819), the only species

Page 422

in this genus, found at 2420 m depth, off Alexandria (Egypt)
(KEEN, 1969).

During 1984 and 1985, the Spanish Institute of Ocean-
ography (I.E.O.) carried out several expeditions to study
the biocoenoses of the red coral bottoms in the Alboran
Sea, between about 50 and 200 m. Within the bivalve
taxocoenoses from the expeditions of 1984, only Corallio-
phaga lithophagella was collected (SALAS & SIERRA, 1986).
However in March 1985, we found one specimen of C.
coralliophaga (Gmelin, 1791) inside red coral stones from
around Alboran Island (35°54’-35°52'N, 3°09'-3°05'W),
which had some remains of the red coral Corallium rubrum
(Linnaeus, 1758). This specimen was collected dead; a
small drill hole was present in the valve. We were able to
confirm the identification by comparing it with three lots
of Coralliophaga coralliophaga from the National Museum
of Natural History (NMNH), Smithsonian Institution
(Washington).

According to ABBOTT (1974), Coralliophaga coralliopha-
ga occurs in America from North Carolina to Texas and
in the West Indies, Bermuda, and Brazil. The lots in the
NMNH are from the Indo-Pacific area—Caroline Islands
(USNM 634489; USNM 634506), Gilbert Islands
(USNM 608983), Red Sea (USNM 608869)—and Japan
(USNM 345022). They have always been found in coral
reefs.

Morris (1984) does not note this species in the Red
Sea, listing only two species of Trapezium: T. oblongum
(Linnaeus, 1758) and 7. bicarinatum (Schumacher, 1817).

Coralliophaga coralliophaga is elongate, with the um-
bones at the anterior end. The shell is yellowish white and
finely sculptured, with radial threads and concentric la-
mellations at the posterior end. This is an uncommon
species, which lives in the burrows of other rock-boring
mollusks. It ranges in size from about 1 to 5 cm (ABBOTT,
1974). The hinge of this species has two parallel, slender
cardinals and one posterior lateral in each valve. The two
muscle scars are unequal, with the posterior being larger
and more elongate. There is a large pallial line, and a
small pallial sinus.

In our 7-mm long shell, the lateral teeth are very weak,
like a lateral ridge, and radial sculpture is absent.

Coralliophaga lithophagella differs from C. coralliophaga
by: (a) the outline of the shell, which in the former is
higher, trapezoidal, and without radial sculpture; (b) the
hinge, which bears the two cardinal teeth (in each valve)
which are larger and divergent (there are no lateral teeth);
and (c) the pallial sinus is less deep and it is posteriorly
closed by the pallial line.

Acknowledgments

We express our appreciation to the Spanish Institute of
Oceanography (1.E.O.) and to Dr. J. Templado for send-
ing us the bivalve material from the Red-Coral Expeditions
in the Alboran Sea. Also, we are grateful to Miss Diane
Bohmhauer, Museum Specialist (Mollusks) of the Smith-
sonian Institution (NMNH), for sending us the lots of

The Veliger, Vol. 30, No. 4

Coralliophaga coralliophaga and indicating the geographic
distribution of the Smithsonian collections of this species.

Literature Cited

ABBOTT, R.T. 1974. American seashells. 2nd ed. Van Nostrand
Reinhold Co.: New York. 663 pp., 24 color pls.

FRANC, A. 1960. Classe des Bivalves. Pp. 1845-2164. In: P.
P. Grasse, Traité de zoologie, T.V (II). Ed. Masson & Cie.
2164 pp.

KEEN, M.A. 1969. Family Trapeziidae, Lamy 1920. Pp. N655-
N657, fig. E132. In: R. C. Moore (ed.), Treatise on inver-
tebrate paleontology, L. C. Cox et al., Part N (Bivalvia) 2:
491-952. Geol. Soc. Amer. & Uniy. Kansas: Lawrence, Kan-
sas.

Morris, S. 1984. Bivalves. Pls. 38-49. In: D. Sharabati (ed.),
Red Sea shells. KPI Limited Routletge & Kegan Paul Plc:
London.

NorpDsIECK, F. 1969. Die europaischen Meeresmascheln (Bi-
valvia) von Eismeer bis Kapverden Mittelmeer und Schwarzes
Meer. Gustav Fischer Verlag Ed.: Stuttgart. 256 pp.; 25 pls.

PIANI, P. 1980. Catalogo dei Molluschi Conchiferi viventi nel
Mediterraneo. Boll. Malacol., Milano 16(5/6):113-224.

Saas, C. & A. SIERRA. 1986. Contribution to the knowledge
of the molluscs bivalves from the red coral bottoms of the
Alboran Island (Spain). Iberus 6(II):189-200; 1 pl.

Harpidae Bronn, 1849 (Gastropoda):
Conserved by ICZN
by
William K. Emerson
Department of Invertebrates,
American Museum of Natural History,
New York, New York 10024, U.S.A.
and
Roger N. Hughes
School of Animal Biology,
University College of North Wales,
Bangor, Gwynedd LL57 2 UW, U.K.

In a recent paper on the anatomy and taxonomy of the
gastropod genera Harpa and Morum, we (HUGHES &
EMERSON, 1987:357) accepted RAVEN’s (1985) proposal
to use Harpaidae as an emended name to replace Harpidae
Bronn, 1849 (type genus Harpa Roding, 1798), not Har-
pidae Hawle & Corda, 1847 (type genus Harpes Goldfuss,
1839, in Trilobita). We noted that final acceptance of the
emended name Harpaidae would have to await action by
the International Commission on Zoological Nomencla-
ture to remove the homonymy. Subsequently, the Com-
mission (ICZN, 1987) ruled by order of Opinion 1436 to
place on the Official List of Family-Group Names in Zo-
ology the names Harpidae Bronn, 1849, type genus Harpa
Réding, 1798 (Gastropoda) and Harpetidae Hawle &
Corda, 1847 (an emendation under the plenary powers of
“Harpides’’), type genus Harpes Goldfuss, 1839 (Trilo-
bita). As a result of this action, the familial name Harpidae
is available in its accustomed sense in the Neogastropoda
and the emended names Harpaidae and Harpainae are
now superfluous.

Notes, Information & News

Page 423

Literature Cited

BRONN, H.G. 1849. Handbuch der Geschichte der Natur, 3(3)
Index Palaeontologicus. Stuttgart. 980 pp.

Go.pruss, G. A. 1839. Beitrage zur Petrefactenkunde. Nova
Acta Acad. Caes. Leop. Carol. 19(1):358-359.

HawLg, I. & A. J. C. Corba. 1847. Prodrom einer Mono-
graphie der Bohmischen Trilobiten. K. Bohm. Gesell. Wiss.
(Prague), (Abhandl.) 5:1-176.

Hucues, R. N. & W. K. EMERSON. 1987. Anatomical and
taxonomic characters of Harpa and Morum (Neogastropoda:
Harpaidae). Veliger 29(4):349-358.

ICZN. 1987. Opinion 1436, Harpidae Hawle & Corda, 1847
(Trilobita) and Harpidae Bronn, 1849 (Mollusca, Gastro-
poda): a ruling to remove the homonymy. Bull. Zool. Nom.
44(2):137-138.

RAVEN, J. G. M. 1985. Homonymy in the families Harpidae
Hawle & Corda, 1847 (Trilobita) and Harpidae Bronn,
1849 (Mollusca, Gastropoda). Z.N.(S.)2331. Bull. Zool.
Nom. 42(1):79-80.

ROpING, P. F. 1798. Museum Boltenianum, part 2. Hamburg.
vill + 199 pp.

A Note on Unjustified Emendations
by
Rudiger Bieler
Smithsonian Marine Station at Link Port,
5612 Old Dixie Highway,
Fort Pierce, Florida 34946, U.S.A.

There seems to be some misunderstanding in recent lit-
erature about the status of the “Appendix D: Recommen-
dations on the Formation of Names” in the International
Code of Zoological Nomenclature. These recommenda-
tions are appended to the rules, and are “provided as a
guide to good usage in nomenclature. They do not have
the force of rules” (ICZN, 1964:93; ICZN, 1985:181; see
also p. 1 in either edition). They are meant to serve as
guidelines for the original describer of a taxon, and, among
other things, they suggest that the prefix “mac” be used
instead of “Mac,” “Mc,” or “M,” when a zoological name
is formed (ICZN, 1985:197).

The following are three examples of instances in which
authors use this recommendation while citing “the rules”
to emend such names.

OrTIz-Corpes (1983) listed Petaloconchus erectus mac-
ginty: Olsson & Harbison, 1953, and stated (1983:56): “I
am modifying mcginty: to macginty: to conform it to the
rules of Zoological Nomenclature.”

CLARKE (1986:92) stated “ICZN Rules require that
Elliptio memichaeli, as originally proposed [by Clench &
Turner, 1956], should be emended to Elliptio macmi-
chaelt.”

Another name change by OrTIZ-Corps (1983:170) is a
little more complicated. He emended the original spelling
of Atys m’andrewu E. A. Smith, 1872, to Atys macandrewn,
“to conform it to the International Code of Zoological
Nomenclature (Article 27, p. 29; p. 109)” (ORTIZ-Corps,
1983:171). The references given by Ortiz-Corps refer to

the then valid second edition of the Code (ICZN, 1964),
specifically to Article 27 (‘no diacritic mark, apostrophe,
or diaeresis is to be used . . .”) and to the recommendations
concerning prefixes as described above. In both the old
(2nd) and new (3rd) editions of the Code, there are pro-
visions to emend original spellings that contain diacritic
marks, apostrophes, diaereses, or hyphens (ICZN, 1964:
Art. 32(c)(i); ICZN, 1985:Art. 32(d)(i)). However, the
text in that article reads “A name published with ...
apostrophe is to be corrected ... by the deletion of the
mark concerned and by uniting any resulting parts.”
Therefore, Atys mandrewu is the required, justified emen-
dation of A. m’andrewu; Ortiz-Corps’ Atys macandrewit is
not.

Unfortunately such unjustified emendations cannot be
ignored by subsequent authors, since they are available
names according to the Code: “‘. .. the name thus emended
is available with its own author and date and is a junior
objective synonym of the name in its original spelling; it
enters into homonymy and can be used as a replacement
name” (ICZN, 1985:Art. 33b(iii)).

Thus, careless emendations can produce “instant syn-
onyms” that have to be carried through subsequent lit-
erature. Although not intended by the authors in the above-
mentioned cases, these actions could have resulted in the
introduction of three invalid, but available, new nominal
taxa, Petaloconchus erectus macginty: Ortiz-Corps, 1983,
Atys macandrewu Ortiz-Corps, 1983, and Elliptio macmi-
chaeli Clarke, 1986! I write “could have resulted,” because
there is a further complicating factor that warrants indi-
vidual checking of each case. Although the act of emen-
dation was stressed by each author, they were not neces-
sarily the first to take that action. Atys m’andrewii, for
instance, was changed to macandrewi (sic) at least twice
before, by VON MARTENS (1872:140) and by ODHNER
(1931:24) (the use of the suffix -i for -11 has no nomen-
clatural bearing and is to be treated as an incorrect sub-
sequent spelling, even if the change was deliberate; ICZN,
1985: Art. 33(d)).

Such emendations are not merely not required by the
Code—they are unjustified, cause confusion, and burden
the literature with junior synonyms.

Acknowledgments

I thank Paula M. Mikkelsen, Harbor Branch Oceano-
graphic Institution, Fort Pierce, Richard E. Petit, North
Myrtle Beach, and two anonymous reviewers for helpful
comments on the manuscript.

Literature Cited

CuarRKE, A. H. 1986. Elliptio judithae, new species (Bivalvia,
Unionidae) from the Neuse River, North Carolina. Mal-
acology Data Net (Ecosearch Series) 1(4):78-96.

INTERNATIONAL COMMISSION on ZOOLOGICAL NOMENCLATURE
(ICZN). 1964. International Code of Zoological Nomen-
clature. 2nd ed. London. xix (+1) + 176 pp.

INTERNATIONAL COMMISSION on ZOOLOGICAL NOMENCLATURE

Page 424

(ICZN). 1985. International Code of Zoological Nomen-
clature. 3rd ed. London, Berkeley, and Los Angeles. xx +
338 pp.

OpuHNER, N. H. 1931. Beitrage zur Malakozoologie der Kan-
arischen Inseln. Lamellibranchien, Cephalopoden, Gastro-
poden. Arkiv for Zoologi 23A(14):1-116, pls. 1-2.

OrtTiz-Corps, E. 1983. An annotated checklist of the Recent
marine Gastropoda (Mollusca) from Puerto Rico. Memorias
del Quinto Simposio de la Fauna de Puerto Rico y el Caribe.
Humacao, Puerto Rico. i + 220 pp.

VON MarTENS, E. 1872. Mollusca. Zoological Record for 1872,
9:103-174.

Note on Leaflets in Malacology
by
Richard E. Petit
806 St. Charles Road, North Myrtle Beach,
South Carolina 29582, U.S.A.

Leaflets in Malacology was privately published by the late
S. S. Berry, with 26 numbers issued between 1946 and
1969 (see HERTZ, 1984, The Festivus 15(Suppl.):1-42).

Among Berry’s papers have been found copies of Leaflets
No. 13, with an accompanying note in Berry’s handwriting
stating that “these are the suppressed first printing but
can be used as work copies & rough reprints.” This “sup-
pressed” printing is dated 7 July 1956. The printing that
received distribution is dated 9 July 1956.

The 7 July number, as printed, contained numerous
errors and Berry evidently, and rightfully, felt that it should
be reprinted. Comparison of the page proof of the first
printing shows that the printer corrected most, but not all,
of the errors.

Several dozen copies of this 7 July printing exist, most
with corrections made thereon by Berry. Considering the
state of Berry’s effects during the last few years of his life,
it is possible that copies of the 7 July printing were in-
advertently distributed. Since we have it in Berry’s own
hand that the 7 July printing was suppressed, Leaflets No.
13 cannot be considered to have been published, in the
sense of the /nternational Code of Zoological Nomenclature,
on 7 July, and the actual publication date is 9 July as
shown on the revised printing.

Berry’s note, the page proof, and all copies of the 7 July
printing that have been located are now in the Santa Bar-
bara Museum of Natural History.

International Commission on Zoological Nomenclature
Official Lists and Indexes of Names and
Works in Zoology

A revised and updated edition of the Official Lists and
Indexes of Names and Works in Zoology has now been pub-
lished. For the first time all the names and works on which
the International Commission on Zoological Nomencla-

The Veliger, Vol. 30, No. 4

ture has ruled since it was set up in 1895 are brought
together in a single volume. Entries are arranged in four
sections giving in alphabetical order the family-group
names, generic names, specific names and titles of works
which have been placed on the Official Lists or the Official
Indexes. There are about 9900 entries of which 134 are
for works. In addition, there is a full systematic index and
a reference list to all relevant Opinions and Directions.
The volume is 366 pages, size A4, casebound.
Copies can be ordered from:

The International Trust for Zoological Nomenclature, %
British Museum (Natural History), Cromwell Road, Lon-
don SW7 5BD, U.K. Price £60 or $110 or

The American Association for Zoological Nomenclature,
% NHB Stop 163, National Museum of Natural History,
Washington DC 20560, U.S.A. Price $110 ($100 to mem-
bers of A.A.Z.N.).

California Malacozoological Society

California Malacozoological Society, Inc., is a non-profit
educational corporation (Articles of Incorporation No.
463389 were filed 6 January 1964 in the office of the
Secretary of State). The Society publishes a scientific quar-
terly, The Veliger. Donations to the Society are used to
pay a part of the production costs and thus to keep the
subscription rate at a minimum. Donors may designate
the Fund to which their contribution is to be credited:
Operating Fund (available for current production); Sav-
ings Fund (available only for specified purposes, such as
publication of especially long and significant papers); or
Endowment Fund (the income from which is available.
The principal is irrevocably dedicated to scientific and
educational purposes). Unassigned donations will be used
according to greatest need.

Contributions to the C.M.S., Inc., are deductible by
donors as provided in section 170 of the Internal Revenue
Code (for Federal income tax purposes). Bequests, lega-
cies, gifts, and devises are deductible for Federal estate and
gift tax purposes under sections 2055, 2106, and 2522 of
the Code. Upon request, the Treasurer of the C.M.S., Inc.,
will issue suitable receipts which may be used by donors
to substantiate their tax deductions.

Subscription Rates and Membership Dues

At its regular Annual Business Meeting on 8 October
1987, the Executive Board of the California Malacozoo-
logical Society, Inc., set the subscription rates and mem-
bership dues for Volume 31 of The Veliger. For affiliate
members of the Society, the subscription rate for Volume
31 will be US$28.00; this now includes postage to domestic
addresses. For libraries and nonmembers the subscription
rate will be US$56.00, also now with postage to domestic
addresses included. An additional US$4.00 is required for

Notes, Information & News

all subscriptions sent to foreign addresses, including Can-
ada and Mexico.

Affiliate membership in the California Malacozoologi-
cal Society is open to persons (no institutional member-
ships) interested in any aspect of malacology. There is a
one-time membership fee of US$2.00, after payment of
which, membership is maintained in good standing by the
timely renewal of the subscription.

Send all business correspondence, including subscription
orders, membership applications, payments for them, and
changes of address to C.M.S., Inc., P.O. Box 9977, Berke-
ley, CA 94709.

Page Charges

Although we would like to publish papers without charge,
high costs of publication require that we ask authors to
defray a portion of the cost of publishing their papers in
The Veliger. We wish, however, to avoid possible financial
handicap to younger contributors, or others without fi-
nancial means, and to have charges fall most heavily on
those who can best afford them. Therefore, the following
voluntary charges have been adopted by the Executive
Board of the California Malacozoological Society: $30 per
printed page for authors with grant or institutional support
and $10 per page for authors who must pay from personal
funds (2.5 manuscript pages produce about 1 printed page).
In addition to page charges, authors of papers containing
an extraordinary number of tables and figures should ex-
pect to be billed for these excess tables and figures at cost.
It should be noted that even at the highest rate of $30 per
page the Society is subsidizing well over half of the pub-
lication cost of a paper. However, authors for whom the
regular page charges would present a financial handicap
should so state in a letter accompanying the original manu-
script. The letter will be considered an application to the
Society for a grant to cover necessary publication costs.

We emphasize that these are voluntary page charges and
that they are unrelated to acceptance or rejection of manu-
scripts for The Veliger. Acceptance is entirely on the basis
of merit of the manuscript, and charges are to be paid after
publication of the manuscript, if at all. Because these con-
tributions are voluntary, they may be considered by authors
as tax deductible donations to the Society. Such contri-
butions are necessary, however, for the continued good
financial health of the Society, and thus the continued
publication of The Veliger.

Reprints

While it was hoped at the “birth” of The Veliger that a
modest number of reprints could be supplied to authors
free of charge, this has not yet become possible. Reprints
are supplied to authors at cost, and requests for reprints
should be addressed directly to the authors concerned. The
Society does not maintain stocks of reprints and also cannot

Page 425

undertake to forward requests for reprints to the author(s)
concerned.

Patronage Groups

Since the inception of The Veliger in 1958, many generous
people, organizations, and institutions have given our jour-
nal substantial support in the form of monetary donations,
either to The Veliger Endowment Fund, The Veliger Op-
erating Fund, or to be used at our discretion. This help
has been instrumental in maintaining the high quality of
the journal, especially in view of the rapidly rising costs
of production.

At a recent Executive Board Meeting, we felt we should
find a way to give much-deserved recognition to those past
and future donors who so evidently have our best interests
at heart. At the same time, we wish to broaden the basis
of financial support for The Veliger, and thus to serve our
purpose of fostering malacological research and publica-
tion. Accordingly, it was decided to publicly honor our
friends and donors. Henceforth, donors of $1000.00 or
more will automatically become known as Patrons of The
Veliger, donors of $500.00 or more will be known as Spon-
sors of The Veliger, and those giving $100.00 or more will
become Benefactors of The Veliger. Lesser donations are
also sincerely encouraged, and those donors will be known
as Friends of The Veliger. To recognize continuing support
from our benefactors, membership in a patronage category
is cumulative, and donors will be listed at the highest
applicable category. As a partial expression of our grati-
tude, the names only of donors in these different categories
will be listed in a regular issue of the journal. Of course,
we will honor the wishes of any donor who would like to
remain anonymous. The Treasurer of the California Mal-
acozoological Society will provide each donor of $10.00 or
more with a receipt that may be used for tax purposes.

We thank all past and future donors for their truly
helpful support and interest in the Society and The Veliger.
Through that support, donors participate directly and im-
portantly in producing a journal of high quality, one of
which we all can be proud.

Notes to Prospective Authors

The increasing use of computers to prepare manuscript
copy prompts the following notes. We request that the
right margin of submitted papers be prepared “ragged,”
that is, not justified. Although right-justified margins on
printed copy sometimes look “neater,” the irregular spac-
ing that results between words makes the reviewer’s, ed-
itor’s, and printer’s tasks more difficult and subject to error.
Similarly, the automatic hyphenation capability of many
machines makes for additional editorial work and potential
confusion; it is best not to hyphenate words at the end of
a line. Above all, manuscripts should be printed with a

Page 426

printer that yields unambiguous, high-quality copy. With
some printers, especially some of the dot-matrix kinds,
copy is generally difficult to read and, specifically, the
letters “a, p, g, and q” are difficult to distinguish, especially
when underlined as for scientific names; again, errors may
result.

Other reminders are (1) that three copies of everything
(figures, tables, and text) should be submitted to speed the
review process, and (2) absolutely everything should be
double-spaced, including tables, references, and figure leg-
ends.

Because The Veliger is an international journal, we oc-
casionally receive inquiries as to whether papers in lan-
guages other than English are acceptable. Our policy is
that manuscripts must be in English. In addition, authors
whose first language is other than English should seek the
assistance of a colleague who is fluent in English before
submitting a manuscript.

Moving?

If your address is changed it will be important to notify
us of the new address at least six weeks before the effective
date and not less than six weeks before our regular mailing
dates. Send notification to C.M.S., Inc., P.O. Box 9977,
Berkeley, CA 94709.

Because of a number of drastic changes in the regulations
affecting second class mailing, there is now a sizable charge
to us on the returned copies as well as for our remailing

The Veliger, Vol. 30, No. 4

to the new address. We are forced to ask our members and
subscribers for reimbursement of these charges:

change of address and re-mailing of a returned issue—

$5.00.

Sale of C.M.S. Publications

All back volumes still in print, both paper-covered and
cloth-bound, are available only through “The Shell Cab-
inet, 12991 Bristow Road, Nokesville, VA 22123. The
same applies to the supplements still in print, with certain
exceptions (see below). Prices of available items may be
obtained by applying to Mr. Morgan Breeden at the above
address.
Volumes 1 through 13, 24, 26, and 27 are out of print.
Supplements still available are: part 1 and part 2, sup-
plement to Volume 3, and supplements to Volumes 7, 11,
14, 15, and 16; these can be purchased from “The Shell
Cabinet” only. Copies of the supplement to Volume 17
(“Growth rates, depth preference and ecological succession
of some sessile marine invertebrates in Monterey Harbor”
by E. C. Haderlie) may be obtained by applying to Dr.
E. C. Haderlie, U.S. Naval Post-Graduate School, Mon-
terey, CA 93940.
Single copies of back issues of the The Veliger still in
print are available excluswely from:
Conchylien Cabinet,
Grillparzerstrasse 22,
D-6200 Wiesbaden, BRD (West Germany).

Student Research Grant in Malacology

The Santa Barbara Shell Club has announced the availability of funds to support student research
in malacology through the Sara T. DeLaney Scholarship.

The successful applicant must be a full-time student in a formal graduate degree program, and the
thesis topic must be primarily focused on some aspect of eastern Pacific or west American malacology
(including marine, freshwater, or terrestrial mollusks).

The following documents are required for each application: (1) A proposal, limited to three pages,
that discusses the research project and details the work to be aided by this grant and its malacological
significance; (2) A budget that outlines how these funds will be used; (3) A curriculum vita or resume;
(4) A letter of recommendation from the applicant’s thesis advisor; and (5) A list of grants and amounts
that are currently being received or are anticipated to be received in the 1988-89 academic year.

A single research grant of up to $1000 is available. Funds are available for the purchase of research
materials, usage fees (electron microscope and computer), and travel costs to museums or institutions

having resources vital to the research topic.

Completed applications must be received no later than 1 June 1988. Please send to:

Sara T. DeLaney Scholarship
Santa Barbara Shell Club

P.O. Box 30191

Santa Barbara, CA 93130.

For further information, contact Paul Scott (805) 682-4711.

The Veliger 30(4):427 (April 1, 1988)

THE VELIGER
© CMS, Inc., 1988

BOOKS, PERIODICALS & PAMPHLETS

Two New Audio Cassettes Say It Right!

by R. TuckKEeR ABBoTT. 1987. American Malacologists,
P.O. Box 1192, Burlington, MA 01803. Stereo cassette,
35 min. Price: $7.90 plus $2.10 for shipping.

On Say it right! How to pronounce the scientific names of
Seashells of North America R. Tucker Abbott pronounces
the Latin, scientific names of 1250 species of mollusks from
both coasts of North America. The list is from the index
of the 1986 revised edition of Abbott’s Seashells of North
America, and also includes some names of authors, family
names, and technical terms. The tape begins with the
important note that there is no one “correct” pronuncia-
tion, only a “customary” one, and even this may vary from
region to region.

If the tape encourages someone with a fear of scientific
names to plunge ahead and use them, then it will have
served a fine purpose. The format of a tape cassette, how-
ever, seems rather cumbersome and limited. I do not keep
a cassette player handy and indeed had to listen to the tape
in my car! Some assistance is provided for finding a par-
ticular name of interest by means of an index keyed to a
tape counter.

Some seekers of information on customary pronuncia-
tion of scientific names will undoubtedly appreciate hear-
ing someone actually pronounce the names in question
(and Abbott’s voice is a pleasant one). Others may prefer
the visual, phonetic approach taken in the book /t’s Easy
to Say Crepidula by J. M. Cate & S. Raskin reviewed in
the July 1987 issue of The Veliger.

D. W. Phillips

Exploring Collectible Shells

by R. TuckER ApBpBoTtT. 1987. American Malacologists,
P.O. Box 1192, Burlington, MA 01803. 90-min cassette,
and 64-pp paperback book. Total price for cassette and
book: $12.95, postage included.

The tape is a 90-min commentary keyed, page by page,
to the included book by Abbott, Collectible Shells of the

Southeastern U.S., Bahamas & Caribbean. The book is a
nicely produced, all-color guide to mollusks of Florida and
the Caribbean, which includes in addition to the many
plates of Recent mollusks some information on fossils and
how to collect, clean, and store shells. The tape contains
additional information on the habits and uses of the mol-
lusks pictured.

D. W. Phillips

Marine Invertebrates of the Pacific Northwest

by EUGENE N. KOZLOFF. 1987 (actually published 24 Feb-
ruary 1988. University of Washington Press: Seattle, Wash.
520 pp. Price: $35.

This is a greatly expanded second edition of Kozloff’s
1974 “Keys to the Marine Invertebrates of Puget Sound,
the San Juan Archipelago, and Adjacent Regions.” It is
more than double in size, set in better type, printed on
better paper, and has many more illustrations. It is de-
signed as an identification manual and key to some of the
more important taxonomic literature.

The Mollusca are covered on 112 pages (pp. 184-295)
in four chapters with 188 illustrations, including many
photographs. This is in contrast to the 55 pages and 21
line drawings of the first edition. Of course, only a rela-
tively small proportion of the species keyed could be il-
lustrated, even in the expanded book.

The quality of particular parts of the molluscan coverage
depends on whether a specialist was found to help and
whether relevant literature was located. Thus, Hochberg’s
treatment of the cephalopods, Marshall & Shimek’s cov-
erage of the scaphopods, and Shimek’s work on the Tur-
ridae are especially good. The limpets show the advice of
David Lindberg and the chitons that of the late Tony
Ferreira. However, the Rissoidae/Rissoinidae show that
Ponder’s (1985) key paper has been missed.

The Mollusca seem relatively error free, though I spot-
ted Tellina “‘nucleoides” instead of 7. nuculoides.

Gene Coan

ve rep: sare soit
ihe wh Bae Vi

ya

VaR!

eel

Information for Contributors

Manuscripts

Manuscripts must be typed on white paper, 812” by 11”, and double-spaced throughout
(including references, figure legends, footnotes, and tables). If computer generated copy
is to be submitted, margins should be ragged right (7.e., not justified). To facilitate the
review process, manuscripts, including figures, should be submitted in triplicate. The
first mention in the text of the scientific name of a species should be accompanied by the
taxonomic authority, including the year, if possible. Underline scientific names and other
words to be printed in italics. Metric and Celsius units are to be used.

The sequence of manuscript components should be as follows in most cases: title page,
abstract, introduction, materials and methods, results, discussion, acknowledgments, lit-
erature cited, figure legends, figures, footnotes, and tables. The title page should be on a
separate sheet and should include the title, author’s name, and address. The abstract
should describe in the briefest possible way (normally less than 200 words) the scope,
main results, and conclusions of the paper.

Literature cited

References in the text should be given by the name of the author(s) followed by the
date of publication: for one author (Smith, 1951), for two authors (Smith & Jones, 1952),
and for more than two (Smith et al., 1953).

The “literature cited” section must include all (but not additional) references quoted
in the text. References should be listed in alphabetical order and typed on sheets separate
from the text. Each citation must be complete and in the following form:

a) Periodicals
Cate, J. M. 1962. On the identifications of five Pacific Mitra. Veliger 4:132-134.

b) Books

Yonge, C. M. & T. E. Thompson. 1976. Living marine molluscs. Collins: London.
288 pp.

c) Composite works

Feder, H. M. 1980. Asteroidea: the sea stars. Pp. 117-135. In: R. H. Morris, D. P.
Abbott & E. C. Haderlie (eds.), Intertidal invertebrates of California. Stanford Univ.
Press: Stanford, Calif.

Tables
Tables must be numbered and each typed on a separate sheet. Each table should be
headed by a brief legend.

Figures and plates

Figures must be carefully prepared and should be submitted ready for publication.
Each should have a short legend, listed on a sheet following the literature cited.

Text figures should be in black ink and completely lettered. Keep in mind page format
and column size when designing figures.

Photographs for half-tone plates must be of good quality. They should be trimmed off
squarely, arranged into plates, and mounted on suitable drawing board. Where necessary,
a scale should be put on the actual figure. Preferably, photographs should be in the
desired final size.

It is the author’s responsibility that lettering is legible after final reduction (if any)
and that lettering size is appropriate to the figure. Charges will be made for necessary
alterations.

Processing of manuscripts

Upon receipt each manuscript is critically evaluated by at least two referees. Based on
these evaluations the editor decides on acceptance or rejection. Acceptable manuscripts
are returned to the author for consideration of comments and criticisms, and a finalized
manuscript is sent to press. The author will receive from the printer two sets of proofs,
which should be corrected carefully for printing errors. At this stage, stylistic changes
are no longer appropriate, and changes other than the correction of printing errors will
be charged to the author at cost. One set of corrected proofs should be returned to the
editor.

An order form for the purchase of reprints will accompany proofs. If reprints are
desired, they are to be ordered directly from the printer.

Send manuscripts, proofs, and correspondence regarding editorial matters to: Dr. David W.

Phillips, Editor, 2410 Oakenshield Road, Davis, CA 95616 USA.

CONTENTS — Continued

The gastropods in the streams and rivers of five Fiji Islands: Vanua Levu, Ovalau,
Gau, Kadavu, and Taveuni.
AX. “ETAYINES 303 550 Go Shy 58 sav PB ens oe satis gah 9 Gc ET eI Re aust

New molluscan hosts for two shrimps and two crabs on the coast of Baja
California, with some remarks on distribution.
ERNESTO) GAMPOS- GONZATEZ) Sie ine ee eee ee ee

Systematics of the Scurriini (new tribe) of the northeastern Pacific Ocean
(Patellogastropoda: Lottiidae).
DAVID Re EINDBERG 932.01) 354s ai ote ions a ae So ne

Anatomy and zoogeography of Glossodoris sedna and Chromodoris grahami
(Opisthobranchia: Nudibranchia) in the tropical western Atlantic and
Caribbean. ;

FANS. BER TSGH (5 iyi5 se! S05 ice ay Oe Se are en ea ea

A new fossil Cypraea (Gastropoda: Prosobranchia) from southern Africa with
notes on the Alexandria Formation.
WIE DTAM) Rese TDsviEDVAND Men Goel BX © Wc aa ae

Two new species of Liotiinae (Gastropoda: Turbinidae) from the Philippine
Islands.
JAMESUED | MIGIGEAN 23) 5 37: GRR See einen anteare ieee ON Mie eek et pe. 9 Sn ae

Six new species of Terebridae (Mollusca: Gastropoda) from Panama and the
Indo-West Pacific.
(PWIRAVBRAM@HER 277.0." h ch. (ay seater eles nelle! tase YORI) 5.00 Chas, Cee

Assignment to genus Naesiotus (Albers, 1850) of several species formerly assigned
to Rabdotus (Albers, 1850) (Gastropoda: Pulmonata: Bulimulidae).
AMES Ex RIORRMANE 5/02 sci haat omer ee pope en ee gene NAS AIR ea

NOTES, INFORMATION & NEWS

Mexichromis tura: range extension of a rarely observed nudibranch.
AGEX@ISERSTILCHEAND IANS BERS CEs eae ee ee ee

New record of the coral clam Coralliophaga coralliophaga (Gmelin, 1791)
(Bivalvia: Trapezidae) in the Mediterranean Sea.
CARMEN SALAS, AGUSTIN BARRAJON, AND FRANCISCO CARPENA .......

Harpidae Bronn, 1849 (Gastropoda): conserved by ICZN.
WILLIAM K. EMERSON AND ROGER N. HUGHES ....................

A note on unjustified emendations.
RUDIGER: BIRGER ON 0 Daal hid orks. oe one 8 a deed oe eee ee ee

Note on Leaflets in Malacology.
RICHARD EE SRE WIM hg26 57 = pee cc pains ee Sek ae ero UN ie Ra a

b A onan Tt Ta’. ote 2) a Be ony Coe 11 ea BN re Ee a 05 A A eal ot Be ee EBS tant Re per mwa Fly beh at gl dag fly Tae © Taree he ES BOE ed Ne 6) 818 Tae OLS)

NVINOSHILIWS

NVINOSHLIWS
NVINOSHLINS

SS
*

SMITHSONIAN INSTITUTION NOI!LNLILSNI NVINOSHLIWS

SMITHSONIAN
Gy
NVINOSHLIWS

NOILMLILSNI NVINOSHLINS SaI¥vVUdIT LIBRARIES

Saiul

LIBRARIES SMITMSONIAIN

NOILALILSNI
NOILNLILSNI
LIBRARIES

\
LIBRARIES SMITHSONIAN

: NS
INSTITUTION NOILALILSNI NVINOSHLINS S3Iy¥vydtt LIBRARIES SMITHSONIAN

VUdiT LIBRARIES SMITHSONIAN

S3IYVYSIT- LIBRARIES SMITHSONIAN

INSTITUTION NOILNLILSN!
INSTITUTION NOILNLILSNI

INSTITUTION
INSTITUTION
Salauvagit

sSaravaurr
Satu

LIBRARIES SMITHSONIAN

INSTITUTION NOILNLILSNI NVINOSHLINS S3IU%

NOILOLILSN!I NVINOSHLIWS
Hy,
4h ~S

LIBRARIES SMITHSONIAN INSTITUTION NOILALILSNI_ NVINOSHLINS S3IYVYGIT LIBRARIES SMITHSONIAN INSTIT

NVINOSHLINS S3!1YVUGIT_LIBRARIES SMITHSONIAN

Nv NOSHILIVYS ©
SMITHSONIAN
NWINOSHLIWS
SMITHSONIAN
SMITHSONIAN

NWINOSHLINS
\s
SMITHSONIAN
NVINOSHLIWS

As

NOILMILILSNI

LIBRARIES
NOILNLILSNI
LIBRARIES
NOILALILSNI
LIBRARIES
NOILALILSNI

NOILNLILSNI

NOILNLILSNI NVINOSHLINS S31YVYYGIT LIBRARIES SMITHSONIAN INSTITUTION NOILALILSNI NVINOSHLINS S3Iu\

SMITHSONIAN INSTIT

INSTITUTION
Saiuvudit
INSTITUTION
INSTITUTION

INSTITUTION

sgiuvugi
Wy

@ GY

INSTITUTION

ry

LIBRARIES SMITHSONIAN INSTITUTION NOILNLILSNI

Ss saiuvuagii

SJIYWVYEIT LIBRARIES

NVINOSHIINS S3luvudii LIBRARIES

zZ (99)

< = Za fe SZ Z < z
z = = WS 5 z a yf fey Z Zz \S
5 : ENN 2 S 32M 3 aS
x fe) Ws :
: : 2 = 2Oiy = z
; . FL Mnney é Se we 5
,NOMMLILSNI_ NVINOSHLIWS Saluvugit_ LIBRARIES SMITHSONIAN INSTITUTION NOILMLILSNI NVINOSHLINS S31 Uk
em) ze SYS 4 ul ul
a 2 WO 2 <

oe WQ, [aig

= \ mu
2 ae ON S =
jt) =) SS Zz a!

INSTITUTION NOILALILSNI

LIBRARIES SMITHSONIAN SAI¥YVUEIT LIBRARIES

; a
NVINOSHLINS SMITHSONIAN

x 5 7 iss
S32 Ff
IT LIBRARIES

SAIYVYYAIT LIBRARIES
INSTITUTION NOILOLILSNI

INSTITUTION NOILALILSNI

c
<x %
a
{wa}
ia
co z Zz im rd
i fs) S) _ a
pe = = og Se) w
ee 5 5 2 70 Mie)
es Ee E > > i >
Ee oe = a 2 “2
; ie as 3
z zZ 2 om B o
NOILNLILSNI NVINOSHLINS S3IYuVvudl) INSTITUTION NOILALILSNI NVINOSHLINS S3IYY
w z w z a) wily be = rn !
Z Wy Zz = tf, =
2 YY ® 2 YY. % : : 2 Gy? 1g
3 li he 2 8 lol; 2 g 2 8 fF 3 z
Zz j YG fo 4! = 2 4 i= Zz = S , /, Vie 4 E Z, d y
E 2 S = es Se S 5
_LIBRARIES SMITHSONIAN INSTITUTION NOILALILSNI_NVINOSHLINS Saidvugiy LIBRARIES SMITHSONIAN INSTITI
2) = ; = _
2 é uw! & uw 2 us 2
= a 2 co = & = ze =
= < ae < en < 5 2 ee
= : 5 ee = e S cc 5
S) aN rs) ee ) = 3 co 5
z ay Zz aa 2 =) Zz mary 2

ee ee ee 2 a ee i oe
; = = (on) . €& =
OILNLILSNI NVINOSHLIWS °S3 luvugd Mot BRARI ES SMITHSONIAN INSTITUTION MGT ET NUSNVINOSHLNS tes lyVvy
z = y 3s Kx = < 2 << =
z a4, Zw SS = z ar Zz = ah
5 GY 2 QRS g z S we
% SAX hye:
2 Gy = \X\ 3 : g = 2 “iy
G = > = hie) = > = >
o Zz 7) ee oO BA ae a) Zz
IBRARI ES SMITHSONIAN _ REIGN NOME TSNUENVINOSHLINS: “S JIYvegiy Pe MITHSONIAN _ INSTITUT
uw 2 i z SS ra] a ra) 2
«. 7 fy > a = AS al cm . vz
ee, Ye, S a aN YQ Pe Ss oc =
a A re) = 5 Sic fe) = o
= =z a Zz Sh Sy = ear) Zz
OILALILSNI NVINOSHLIWS >o4 1yYvug ive LIBRARI ES_ SMITHSONIAN INSTITUTION a NOILALILSNI _NVINOSHLIWS ~°4 1YVas
! sir fe) = e) x ce o res 2
o S — ow — w a io) > =
re) INN 25 Pe) & 23 5 Be IS NaS
oe ae \ . > = ead i= Beene \ {
=) WYdX = wD — a) = eo) WN =
oS OE oe a ca = ae RQ
a WG = Be a D ae aa
! w aie = w A w z wo as Zz
IBRARIES SMITHSONIAN INSTITUTION NOILALILSNI NVINOSHLIWS LIBRARIES SMITHSONIAN INSTITUT
ER Yn ae « (22) za on ZZ n Zz ’
= < = gy, = = s = Sues
2 Ss \y i 82 : é 2 2 \v
3 2 wNE G4? : 2 é 2h
Z BNO 2 PO Z. = = E NS
= = es : : au ae Ae
SNWINOSHIIWS Slteve ald LIBRARIES SMITHSONIAN INSTITUTION NGITUETI SNS NVINOSHIINS) 34 fyV
: i sh a :
é bs z us a us & a
= za w = w et oc
eat 4 a =I eee
c . < Cc <x = <t Cc ¥
= Ge 4 a = = a ee
5 e 5 = 3 = S 5
| 2 zy 2 3 2 5 2 -
IBRAR!IES SMITHSONIAN INSTITUTION NOILNLILSN!I NVINOSHLINS S3IYVYEIT LIBRARIES SMITHSONIAN INSTITUT
S ae = Le z ~ s &
S 5 La
= * = i) = ow = “0
5. 2 5 ca 5 2 5 2
Es = = ae = > = >
2p) ”Y as ato w
Z E Z rm iz B Z Hs
OILNLILSNI SAIYVYSIT_ LIBRARIES SMITHSONIAN INSTITUTION NOILNLILSNI
= wn Z SAMS n” Zz oS. nw = 2)
= = aes Xs = Si A oS & Sey
: Sj hg ips S 4 NS = z = Pe :
Zip * EGY IRS 3 EGS 29h 3 ee
“yy * 2m =X : : g : 2 ay
GG = > 2 = > = > = >
ij 7) z i) BI ae Tp > Z wn Pz
IBRARIES SMITHSONIAN INSTITUTION NOILNLILSNI NVINOSHLIWS S3IyuVYUaIT _ INSTITUT
| w > wo = (7p) = w >
| us oa a] a u 7 uu E A
a + ae = z aa a HP fon =!
(2 — ce peas o ms Ye. eZ YY, =a,
<x; a < 3 ee a = GH a
a = = = ne = = “Gy =
= S s S a 5 a Ge is
= z —y > per) Ze MS) z
S3IYVYdIT LIBRARIES INSTITUTION NOILONLILSNI NVINOSHLINS S3I1uvHy:
: : z z : : ay ite
—_ a fo) — os
@ = er) = ow = Gee =
Z E 2 = 5 = > We 5
ce = > = 4 > = 2 S\N
a = es) = > Bo) Ss eo) ASN =
= a E i = -~— NX
m 2 m ” m 2 m : \S 2
wo = wo = 7) z w zs
INSTITUTION NOILALILSNI NVINOSHLINS SSIYVYGIT LIBRARIES SMITHSONIAN INSTITUT
” za * w z w : z ~ w Zz .
= oa = wy, = = < = <
= ZEN = Vt ys, = = S =) 2
INN 8 2 ww 8 OZ ? z = & 2
WN QUE E Ss g FAY ee 2 = = =
ae Se S 2 3 5
DILALILSNI_NVINOSHLINS S3IYVYGIT LIBRARIES SMITHSONIAN INSTITUTION a = NVINOSHIINS RS {YyVy
5 = a us z = a "
oe 2, s a = a
_< 4 < 5 ot < =
[aed = « ( fed = o
a 5 a. = a 5 i

bof dhl nd rticitcteel ih S|
Bits Ubu RAM MARU Cus,
EWG rhage stan

Soares

Serene
eaNa nga ts
enone

Samim ientg

SAS ev Oe,
Some.

See
SNe 88 sateen pa aeuwe secre mye
aes,

Mad emp upeieaceiny
cory

Ww mae Seta as Seda
CS aR ER OW yee a
NEES OU deGe AW oueaeimaeo ne oe

sed nen gin eing epererarmumnue cae
Mase ei te Atacama

Naas NA"¥ eat Hecae eine,
errata aoe wey searns

Wee Sa aany eyes tiers

Maren
tenured cn wane

Wet ev eps
cero

5 9
ous a EAP ae
Fears ane

Aare wan pr corsets
ENE derse er apwenenwewigera re
BM UPAON eye yeas wiser

aves Re a a:
CEO RTE errr
Perper sLaens

Wadd Wa agin y
SSN peapeavern
Oe Nt

Se whe Carano:
Ne oe ee 8 ee vay
No Fg HH
Novag tes ane sty

od awe WETS.

ENS WEA RE SAC TA tara

EPA NEB Amt oo ty He
VENTURE WWI GH Gb een

oo

Seenererel erent 3

TAME Sa rt

STS Se yy OL

RINE wee,
vite

Daeeruriors

ciecneneneee
See
et AE IE nae
Henig atpeithae yal
SRNR VY ai

NA Atonna re
an tueens
Perera
1S open aud esti ee
errr
Iniwaas
ae CL eey evo
pet
SVaswwanrenrien pr
Peasy ear anGsay eset etetieorte pe
AACN Sa ore Ue

Ny
FOUL ONL pa
Nap waeege
SYREN y,

Misery steare nie

NGAUS Io aweciey olay
Sarit aon ort

eure

ete
NSU Wt eae gu ruin ata wu
VERN HNL FeV S6 G6 Ui Nera umio KAUAI
AEA G sways bp aiehukteotital tae
pis usesyu Wea wae CHUTE NY dag MAE
Cac ani fared ngibasy arnt EQNS Rate
meg a

Seaton
SY eH AER EE Oy
Gore

AUN OE,

Aue a eU AN YM
SUSE TAC OWN
a

wad Na tyEM
NU NUSRAT QWs ev ey
SYRU SUT IRMAWAT RUE Bee Aer

RES hs yee
iL abbh el soars ike
S UAUA Wed Ae EAS

se ren eee Sy att

NECN