MEMOIRES

DU MUSEUM

NATIONAL

D’HISTOIRE

NATURELLE

TOME 162

ZOOLOGIE

1994

Actes de la feme Conference inter nationale

des Polychetes

Coordonne par

]ean-CJaude DAUVIN

Lucien LAUBIER

Donald RE1SH

4 TH INTERNATIONAL

P 0 t T C H A E T E

CONFERENCE

FRANC E

i 9 9 2

Source : MNHN, Paris

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MU&UM

Source : MNHN. Paris

Actes de la 4 erne Conference internationale des Polychetes

4 TH INTERNATIONAL

POLYCHAETE

CONFERENCE

ANGER S

FRANC E

i 9 9 2

Source : MNHN. Paris

ISBN : 2-8565 3-214-4

ISSN : 1243-4442

© Editions du Museum national d’Histoire naturelle, Paris, 1994

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MEMOIRES DU MUSEUM NATIONAL D'HISTOIRE NATURELLE

TOME 162

ZOOLOGIE

Actes de la 4eme Conference Internationale

des Polychetes

Jean-Claude DAUVIN* Lucien LAUBER** Donald J. REISH***

* MustSum national d'Histoire naturelle

Laboratoire de Biologie des InvertSbres marins et Malacologie

57, rue Cuvier

F-75005 Paris

** Institut Oceanographique

Laboratoire de Physiologie des Etres marins

195, rue Saint-Jacques

F-75005 Paris

*** California State University

Department of Biology

Long Beach. CA 90804

USA

EDITIONS

DU MUSEUM

PARIS

1994

Source : MNHN. Paris

Source ; MNHN, Paris

CONTENTS

SOMMAIRE

Preface . 9

Acknowledgements . 10

List of participants . 11

List of reviewers . 15

Obituaries . 17

Pierre Fauvel . 17

Ralph 1. Smith . 19

Pavel V. Ushakov . 19

Douglas P. Wilson . 22

Contributed papers . 25

Cytophysiology, development and reproduction . 29

Genetics and morphology . 81

Phylogeny and taxonomy . 145

Ecology and biogeography . 323

Culture and valorisation . 593

Abstracts . 611

Source

Source : MNHN. Paris

PREFACE

Some eight years ago, Professor Kirkec.aard, former Chairman of the International Polychaete Association

and organizer of the Second International Polychaete Conference, suggested dial France, as a European southern

country, should host the Fourth Conference. We fully agreed on this idea, and decided to prepare a proposal which

was submitted to the Association during the Third International Polychaete Conference held in Long Beach,

August 1989. At tiiis time, one of our main difficulties was the choice of die site for this Conference. For several

reasons, most of die french organizers considered the town of Angers as the most appropriate place: the souvenir of

Pierre Fauvel and of his successor Francois Rullier, die availability of convenient facilities, the assistance of

Patrick GlLLET's laboratory in the Institute for Pure and Applied Research of die University Cadioliquc dc l’Ouest,

the opportunity for attendees to discover and copy rare articles and books from Fauvel's library, die touristic

interest of die surroundings of die town of Angers...

During the Long Beach Conference, the French proposal was presented togedier with two odiers proposals, mid

finally adopted by the Association. In accordance with the discussions in Long Beach, we decided to move the

period of the Conference to die end of July instead of the beginning of September; we also considered the

possibility to organize some sampling visits in French classical marine stations and kept in mind the idea of

widening the scope of the Conference to physiology and endocrinology of Polychaetes. More generally, we

followed one suggestion by David George: such an international Conference should not be restricted to ecology

and taxonomy, but should also consider die group as a biological model, and include applied research such as

zootcchny for polychaete farming or search for active molecules such as nereidin or thelepin. The program of die

Proceedings clearly demonstrates dial diis objective has been achieved.

Following die decision of die International Polychaete Association, an Organization Committee was soon

established in France:

President of the Organizadon Committee: Lucien LAUBIER, Bruxelles

Convener: Patrick GlLLET, Angers

G6rard Bellan, Marseille

Michel Biiaud, Banyuls-sur-Mer

Jean-Claude Dauvin, Paris

Daniel DESBRUYkRES, Brest

Andry DHAINAUT, Lille

Nicole DHAINAUT-COURTOIS, Lille

Yves GRUET, Nantes

Christian RETif-RE, Dinard

Jean Vovelle, Paris

Local organization Committee, University Cadiolique de fOuest, Angers:

Elisabeth AILLERIE, Georges LE GUILLANTON, and Anne-Laure Morvan.

The first announcement was sent at die end of December, 1990. In May 1991, we had received 164 posidve

answers, 80 communications titles and 25 posters. A few weeks later, the same figures were respectively 190, 130

and 60.

The Fourth International Polychaete Conference was held July 27-August 1. 1992, at die Centre de Congas,

Angers, France. A total of 200 members from 32 countries attended the Conference. Sessions were conducted over

Source :

10

PREFACE

a six days period wiih two mid-excursions: to the Loire Valley and to Bourgneuf Bay. Several attendees traveled to

the Laboratoire maritime de Dinard following die Conference.

There were 71 oral presentations and 101 posters. Session topics and posters represented the different themes:

cytophysioiogy, taxonomy and phylogeny, biogeography and ecology, reproduction and development. A special

session was organized on polychaete culture and valorisation. Seventy-nine papers were submitted for publication

and analysed by two different reviewers, and by Donald J. Reish. A total of fourteen papers have been rejected by

die reviewers, but abstracts of .ill communications and posters are included in die Proceedings of die Conference.

Lucien Laubier and Patrick GlLLET

ACKNOWLEDGEMENTS

We gratefully acknowledge the financial support and practical assistance to the Conference provided by the

different ministries and various bodies and scientific institutions:

- Ministfcre des Affaires Etrang£res

- Conseil Regional des Pays de la Loire

- Conseil G6n6ral du Maine et Loire

- Vide d' Angers

- Institut Franyais de Recherche pour I'Exploitation de la Mer (IFREMER)

- Universitd Catholique de l'Ouest (UCO)

- Institut de Recherche Fondamentale et Appliqu6e de 1'UCO

- Museum National d'Histoire Naturclle de Paris,

- Museum d'Histoire Naturellc de Nantes.

Special thanks for their help to Yves Gruet and Christian RETltRE who organized excursions, and to

Elisabeth Aillerie for the programme. Thanks arc also extended to Marie-Annick GRUET, Marie-H616ne GlLLET

and Elisabeth AILLERIE for their kind assistance during the Conference.

Many thanks to the Minitextiles Art group for the exhibition on polychaetes.

A special mention must be addressed to the Laboratoire de Biologie des Invert£br6s Marins et Malacologie du

Museum national d'Histoire naturelle, which provided logistic support during the tedious work of preparation of

die present volume.

Source :

LIST OF PARTICIPANTS

ARGENTINA

Amor Analia (La Plata)

BREMEC Claudia (La Plata)

AUSTRALIA

Hutchings Patricia (Sydney)

BELGIUM

Eeckhaut Igor (Mons)

BRAZIL

Lana Paulo Da Cunha (Parana)

NONATO Edmundo Ferraz (Sao Paulo)

Salvador Bei.untani Lara (Sao Paulo)

Santos Maria Auxiadora (Sergipe)

CANADA

Byers Sheila (Toronto)

Caron Alain (Dinard)

Chi a Fu-shiang (Alberta)

DESROSIERS Gaston (Rimouski)

Fournier Judith A. (Ottawa)

Juniper Kim (Montrdal)

Marsden Joan (Montreal)

Masson Stdphane (Quebec)

Miller Retzer Connie (Vancouver)

Miron Gilles (Quebec)

Olivier Marc (Rimouski)

POCKLINGTON Patricia (Halifax)

Qian Pei-Yuan (Vancouver)

White Caroline (Rimouski)

COLOMBIA

LAVERDE-Castillo Juan Jose Antonio (Bogota)

CROATIA

ZAHTILA Elvis (Rovinj)

DENMARK

Hibye-Jacobsen Danny (Copenhagen)

Feldsgaard Pedersen Torben (Aarhus C.)

Hyllberg Jorgen (Aarhus C.)

Kirkegaard Jorgen Bagger (Copenhagen)

Petersen Mary E. (Copenhagen)

CHILE

Carrasco Franklin D. (Concepcion)

CHINA

Wu Baoling (Qing Dao)

FRANCE

BACHELET Guy (Arcachon)

Baudet Joseph (Nantes)

BELLAN Gerard (Marseille)

Bellan-SaNTINI Denise (Marseille)

Bhaud Michel (Banyuls-sur-Mer)

Cha Jae Hoon (Banyuls-sur-Mer)

Dauvin Jean-Claude (Paris)

DESBRUYfeRES Daniel (Brest)

DHAINAUT Andre (Villeneuve d'Ascq)

DHAINAUT-COURTOIS Nicole (Villeneuve d’Ascq)

DuCHfiNE Jean-Claude (B;uiyuls-sur-Mer)

CiENTIL Franck (Roscoff)

Gillet Patrick (Angers)

Gruet Yves (Nantes)

INTES Andre (Brest)

JOUIN-TOULMOND Claude (Paris)

Lambert R6my (Dinard)

Laubier Lucien (Paris)

LECHAPT Jean -Paul (Dinard)

Marcano Guillermo (Arcachon)

Nozais Christian (Banyuls-sur-Mer)

Parreira dos Santos Paulo Jorge (Arcachon)

Pereira de Souza Santos Lilia (Arcachon)

RETlERE Christian (Dinard)

Salen-Picard Chantal (Marseille)

TlllfiBAUT Eric (Roscoff)

Vovellf. Jean (Paris)

GERMANY

Borowski Christian (Hamburg)

DORRESTEIJN Adriaan (Mainz)

12

LIST OF PARTICIPANTS

Fiege Dieter (Frankfurt)

Fischer Albrecht (Mainz)

OOERKE Helmut (Bremerhaven)

Hardege Jorg Detelf (Oldenburg)

Hofmann Dieter K. (Bochum)

Hus EM ANN Fginhard (Bochum)

Richer Frank (Osnabruck)

Plate Susanne (Bochum)

Purschke Gunter (Osnabruck)

Rosenfeldt Pongchai (Hamburg)

Schmidt Hartmut (Osnabruck)

Westheide Wilfried (Osnabruck)

WlNDOFFER Reinhard (Osnabruck)

WRZESINSKI Olgierd (Hamburg)

GREECE

Arvanitidis Christos (Thessaloniki)

Eleftheriou Anastasios (Iraklio)

Papadopoulou K. Nadia (Iraklio)

SlMBOURA Nomiki (Athfcnes)

INDIA

Ayyakkannu K. (Parangipettai)

INDONESIA

ANDI Isdradjat S. (Aarhus C.)

A Rio Raden (Aarhus C.)

BONEKA Farms B. (Aarhus C.)

Erlambang Tanza (Aarhus C.)

Kaligis G. Fontje (Aarhus C.)

Latama Gunarto (Aarhus C.)

Litaay Magdalena (Aarhus C.)

Ompi Medy (Aarhus C.)

Princ.GENIES Delianis (Aarhus C.)

SlREGAR Yusni I. (Aarhus C.)

Soekendarsi Eddy (Aarhus C.)

TANJUNG Afrizal (Aarhus C.)

YULIANDA Fredinan (Aarhus C.)

IRELAND

Allen Hazel

Grehan Anthony J. (Banyuls-sur-Mer)

ISRAEL

Ben-Eliahu Nechama (Jerusalem)

ITALY

Abbiati Marco (Pisa)

Cantone Grazia (Catania)

C'astelli Alberto (Modena)

Gambi M. Cristina (Napoli)

Giangrande Adriana (Lecce)

Gravina M. Flavia (Roma)

Lardicci Claudio (Pisa)

Petrapoli Angela (Lecce)

Prevedelli Daniela (Modena)

Sanfilippo Rossana (Catania)

Sella Gabriella (Torino)

Somashini Alessandra (Roma)

Sordino Paolo (Napoli)

JAPAN

Sato-Okoshi Waka (Sendai)

MEXIQUE

Diaz Victoria (San Diego)

Leon Gonzalez Jesus Angel de (N. Leon)

Molina-Fuentes Enrique (San Nicolas

de los Garza)

Salazar-Vallejo Sergio I. (Chetumal)

SOLIS-WEISS Vivianne (Mexico)

NETHERLANDS

Hove Harry Ten (Amsterdam)

NORWAY

I Iolte Boerge (Tromsoe)

Jorgensen Lis Lindal (Bergen)

Ouc. Eivind (Grimstad)

POLAND

Sicinski Jacek (Todz)

PORTUGAL

Marques Joao Carlos (Coimbra)

Moreira Maria Helena (Aveiro)

PARDAL Miguel Angelo (Coimbra)

Silva Paula Cristina (Aveiro)

RUSSIA

Britayev Temir (Moscow)

Jirkov Igor A. (Moscow)

TZETLIN Alexander (Moscow)

SPAIN

ALOS Calvo Maria Carmen (Barcelone)

LIST OF PARTICIPANTS

13

Brito Maria Carmen (La Laguna)

Capaccioni-AZZati Romana Y. (Valencia)

CARDEL.L Maria Jos6 (Barcclone)

DUESO Ana (Blancs)

Garcia- Arberas Loreto (Bilbao)

Garcia-Martin Salvador F. (Puerto Real)

JUNOY Juan (Madrid)

Lastra Mariano (Santiago)

Lopez Garcia Eduardo (Madrid)

Mendez Muria (Barcelone)

Nunez Jorge (Islas Canarias)

Pinedo Susana (Blanes)

Rallo Ana (Bilbao)

Sarda Rafael (Blanes)

Sanchez Mata Adoracion (Santiago)

San Martin Guillermo (Madrid)

'Lena Medialdea Jose (Valencia)

Torres Gavila Franco Javier (Buijasso)

Vieitez Jose Manuel (Alcala de I Ienares)

Villora-Moreno Santiago (Valencia)

SWEDEN

Akesson Beitil (Goteborg)

Hide Ragnar (Goteborg)

Pleijel Fredrik (Stockholm)

Sigvaldadoti'IR Elin (Stockholm)

TAIWAN

Chen Chang-Po (Taiwan)

Ms I EH Hwey-Lian (Taipei)

THAILAND

Chantrapornsyl Supot (Aarhus)

Nateewathana Anuwat (Phuket)

TRINIDAD

GOBIN Judith (Plymouth)

UNITED KINGDOM

Bamber Roger (Southampton)

Batten Sonia (Southampton)

Bentley Matt (St Andrews)

Chambers Susan (Edinburg)

Coates Amanda (Scotland)

Cunningham Elaine (Tyne and Wear)

Dixon David R. (Plymouth)

Emson Roland H. (London)

George David (London)

Gibbs Peter E. (Plymouth)

Harris Tegwyn (Exeter)

Kendall Michael (Plymouth)

Knic.ht-Jones Phyllis (Swansea)

Knight-Jones Wyn (Swansea)

Mackie Andrew (Wales)

Muir Alexander lan (London)

Olive Peter James William (Tyne)

Paterson Gordon L. J. (London)

Rowe Grant (Southampton)

THORP Clifford H. (Hampshire)

TURNER Geoffrey Simon ( Tyne and Wear)

Warren Lynda (Cardiff)

Woodham Annette (Edinburgh)

UNITED STATES OF AMERICA

Blake James A. (Woods Hole)

DAUER Daniel (Norfolk)

Fauchald Kristian (Washington)

FlTZHUGH Kirk (Los Angeles)

Hilbig Brigitte (Massachusetts)

Jones Howard (Corvallis)

KiRTLEY David W. (Stuart)

Kudenov Jerry D. (Alaska)

Long Charlene D.

Lovell Lawrence L. (California)

Mac Hugh Damhnait (Santa Cruz)

Martin Ann (Redondo Beach)

Mountford Nancy K. (Lusby)

REISH Donald J. (Long Beach)

Rouse Greg (Washington)

Ruff R. Eugene (Needham)

SCHROEDER Paul C. (Pullmann)

Simon Joseph L. (Tampa)

Smith Ralph I. (Berkeley)

Ward Linda (Washington)

Source : MNHN. Paris

Source : MNHN, Paris

LIST OF REVIEWERS

16

LIST OF REVIEWERS

Olive Peter James William (Tyne)

Paterson Gordon L.J. (London)

Warren Lynda (Cardiff)

UNITED STATES OF AMERICA

Blake James A. (Woods Hole)

Butman Cheryl Ann (Woods Hole)

Fauchald Kristian (Washington)

Fitzhugh Kirk (Los Angeles)

Grass le Frederick (New Brunswick)

Grassle Judith (New Brunswick)

Hilbig Brigitte (Massachusetts)

KUDENOV Jerry D. (Alaska)

Levin Lisa A. (La Jolla)

Maurer Don (Long Beach)

Perkins Thomas H. (St Petersburg)

Pettibone Marian H. (Washington)

REISH Donald J. (Long Beach)

Rouse Greg (Washington)

Schroeder Paul C. (Pullmann)

Simon Joseph L. (Tampa)

Obituaries

Pierre FAUVEL (1866-1958),

his life and research on polychaetous annelids

Patrick GILLET

Laboratoire d'Ecoiogie Animale

Institut de Recherche Fondaincntalc et Appliquee

Univcrsite Catholique de l'Ouest

3. place Andre Leroy, B.P. 808

49008 Angers ccdex 01, France

Pierre Louis Andrd FAUVEL (Fig. 1) est nd h Cherbourg le 8 octobre 1866 de Cldmencc Maihilde Cappe

(1851-1909) et de Auguste Alexandre Fauvel (1821-1867), lieutenant dans la marine frangaise. Pierre Fauvel a

suivi ses 6tudes h l'Universit6 de Caen et fut assistant h la station de recherche de Luc-sur-Mer. Le 29 juin 1897, il

obtint son doctoral h TUniversitd de Paris pour son travail sur les Amphar6tiens. II fut alors nomm6 professeur de

zoologie h I'Universitd Catliolique de l'Ouest, puis Doyen de la Faculty des Sciences en 1942.

II 6tudia les polychfctes de diff6rentes regions du monde et de nombreuses expdditions occanographiqucs telles

que celles de 1'IIirondelle, de la Princesse Alice, du Pourquoi Pas ? et de la Calypso. II d6couvrit de nombreuses

espyces nouvelles dont la plus c616bre est Mercierella enigmatica dScouverte dans le canal de Caen par

M. Mercier. Pierre Fauvel avail remarqud les analogies avec Ficopomatus macrodon et ce n'est que ryccmmcnt

que l'espfece fut rebaptis6e Ficopomatus enigmaticus par TEN Hove & WERDENBURG (1978).

II a public environ 170 articles sur les ann61ides polych^tes et r£dige de nombreuses faunes coniine la Faune de

France el la Faune de I'lnde. Ses travaux les plus importants ont porti5 sur l'anatomie compare des Ar<5nicole$, sur

les otocystes, I'gthologie des Pectinaires et une monographic sur les Amphar6tiens. II obtint de nombreux prix et

distinctions dont le Prix Savigny (1915) de FAcademie des Sciences, le Prix Saintour (1926) de I' Academic des

Sciences, et le Prix Gadeau de Kervillc (1930), de la Soci6t6 Zoologique de France.

Pierre Fauvel fit ggalement des recherches de physiologie et de di<5t6lique humaine. II publia une quarantaine

d'articles sur le regime v6g£tarien, la valeur alimentaire des differents pains et l'excrgtion urique. Sous le

pseudonyme d'Flollow-Rim, il signa dgalement une trentaine d'articles sur le cyclisme. Pierre Fauvel mourut le

12 d6cembre 1958 h l'age de 92 ans. Comme l'ficrivait P. Ushakov le 4 mars 1959 h F. Rullier. “Pierre

Fauvel fut un savant Eminent qui a tant fait pour la connaissance des Polych£tes. Les magniliques ceuvres du

professeur Fauvel nous ont servi h tous dans nos 6tudes comme exemple de recherches taxonomiques”.

Pierre Louis Andr6 Fauvel (Fig. 1) was born in Cherbourg in 1866 of C16mence Matliilde Cappe (1851-

1909) and of Auguste Alexandre Fauvel (1821-1867) lieutenant in the French Marine. He was a student of

biology at the University of Caen and became an assistant at the Luc-sur-Mer research station. On June 29, 1897

he passed his doctorate at die University of Paris for his work on Ampharetidae. He was then appointed Professor

of Zoology at the University Catliolique de l'Ouest, and later Dean of the Faculty of Sciences. He studied

polychaetes from different parts of the world and many expeditions such as Hirondelle, Princesse Alice, Pourquoi-

Pas ? and Calypso. He found numerous new species but the most famous of all is Mercierella (Ficopomatus)

enigmatica discovered in the Channel of Caen by M. MERCIER. He had written many fauna such as die Faune de

France, the Fauna of India and won numerous prizes and distinctions including die Savigny Prize (1915), die

18

OB rill ARIES

Saintour Prize (1926) from the Academy of Sciences and the Ciadeau de Kerville Prize (1930) from the Soci6t6

Zoologique de France. Pierre Fauvel died on December 12, 1958, and Francois RULLIER (1907-1981) succeeded

him in the laboratory.

Fig. 1 . Pierre FAUVEL au debut du siecle

REFERENCES

ANONVME. — Cinquante amices d'enseignemenl a VUniversiU Catholique d' Angers ( 1897-1947 ). M. Pierre Fauvel, Doyen

de la Faculte des Sciences. Editions de 1’Ouest, Angers, 31 pp.

Fage L., 1959. — Pierre Fauvel. 1866-1958. Bull. Mus. nat. Hist, nat., Paris , 2c ser., 31:1.

Fauvel P., 1898. — Rechcrches sur les Ampharclidae. Bull. Scient. France Belgique , 30 : 277-489.

Fauvel P.. 1922. Un nouveau Serpulien d’cau saumatre ( Mercierella n. g. enigmatica n. sp). Bull. Soc. Zool. France ,

48 : 424-430.

GlLLET P., 1992. — Travaux de Pierre Fauvel. Francois Rullier el Louis Amourcux sur les Annelides Polychetes de 1894 a

1985. Bull. Soc. Sc. Nat. Ouest de la France, 14 : 20-36.

RULLIER F., 1959. — M. 1c Doyen Pierre Fauvel. Rev. Fac. Cath. Ouest . 2 : 5-27.

1 EN Hove H.. & J.C.A. Werdenburg, 1978. — A generic revision of the brackish-water serpulid Ficopomalus Southern.

1921 (Polychaeta: Serpulidae) including Mercierella Fauvel, 1923, Sphaeropomatus Treadwell, 1934.

Mercierellopsis Rioja, 1945 and Neopomatus Pilai, 1960. Biol. Bull., 154 : 96-120.

Source :

OBITUARIES

19

Ralph Ingram SMITH

1916-1993

Donald J. RF.ISH

Department of Biology

California State University

Long Beach, California 90840, Etats-Unis

Ralph I. Smith, professor Emeritus of Zoology at the University of California at Berkeley, died on May 12,

1993 in Santa Rosa, California. He collapsed after completing The Human Race; he was revived by emergency

workers, but died a few days later. Professionally he was particularly interested in the physiological adaptations of

intertidal invertebrates including polychaetes.

Ralph was born in Braintree, Massachusetts, on July 3, 1916. He attended Harvard University where he

received his doctorate in 1942 under the direction of John Henry Walsh. Following service in the United States

Army during World War II, he joined the faculty of the Zoology Department at the University of California at

Berkeley, a position he held for 41 years until his retirement in 1987. During his tenure at UC Berkeley he served

a term as department chairman, played a major role in the establishment of the University of California's Bodega

Marine Laboratory, and directed 22 doctoral students.

Ralph emphatically denied being a systematist by any stretch of imagination, but he realized the importance of

systematics. He believed in the importance of knowing and using the correct name of an organism. His interests in

this is evident in his taking over Light's Manual (Intertidal Invertebrates of the Central California Coast)

following the death of Dr. S. F. LIGHT. Later he organized and assembled a similar manual for the Woods Hole

region where is often taught in the summer.

His contributions to the knowledge of polychaetes included developmental studies in the nereids and more

recently in the terebellids. He published many papers on salinity tolerance and chloride regulation in nereids which

was based not only with California species but European species as well. He attended die Third and Fourth

International Polychaete Conferences and contributed papers to both.

His wife Todd of 52 years accompanied Ralph in their many travels which included visiting six continents. In

addition to his wife, he is survived by two sisters, five children, and grandchildren.

Pavel Vladimirovitch USHAKOV

1903-1992

Galina BUZHINSKAJA

Zoological Institute

Russian Academy of Sciences

St. Petersburg. Russia

On 25 February 1992, Dr. Professor Pavel Vladimirovitch Ushakov passed away at the age of 88 of cardiac

deficiency in die House of Science Veterans, Pushkin town, St. Petersburg.

The scope of scientific activity of Prof. P.V. USHAKOV included three fields of knowledge: zoology, marine

biology and oceanography. He published about 250 scientific works; eighty of diem, including diree monographs,

deal with systematics and phytogeny of polychaetes. He organized and participated in many marine expeditions

20

OBITUARIES

covering many different regions of the world's oceans, from the Arctic to the Antarctic Regions. He organized two

marine biological stations in the USSR. His works were widely recognized throughout the world. Scientists of

Australia, UK. USSR, USA, France, Germany, Sri-Lanka, named fifty-five marine organisms after him, i.e.

algae, invertebrates and fishes.

He received the degree of Honoris Causa from Aix-Marseilles II University. In 1972, the Oceanographic

Institute in Paris awarded him the Medal of Prince Albert I of Monaco, its highest international award, for his

works on marine biology. The USSR Geographic Society awarded him the Semenov-Tienshansky Gold Medal in

1958 for his works on the Sea of Okhotsk. The USSR Academy of Sciences awarded him the Pavlovsky Gold

Medal in 1983 for his studies of polychaetes.

P.V. Ushakov was born on 27 June 1903 in St. Petersburg into a family of a lawyer. After finishing a

gymnasium in 1920, he entered the Biological Department of the Physico-Mathematicae Faculty of Petrograd

University. He began his marine biological research as a student in 1921. Together with two young scientists

E.K. Guryanova and I.G. Zaks, he studied bionomy of the intertidal zone of Kola Bay and seasonal variations

of its like. This study became a classical work and was widely recognized by marine biologists.

After graduation from the University, Ushakov worked from 1924-1934 in the State Hydrological Institute,

first as a technician, then as a scientist in the Hydrobiology Department. During 1923-1926, Ushakov headed

small research teams on the Novaya Zemlya islands where Uiey studied coastal marine fauna and fauna of relict

lakes. Until 1935, he took part in different expeditions to the White, Barents, Chuckchee, Okhotsk and Japan

Seas. These expeditions resulted in a number of works including the volumes "Fauna and flora of the Chuckchee

Sea" (1952) published on the initiative and under the editorship of P.V. Ushakov and "The Fauna of the Sea of

Okhotsk and conditions of its existence" (1953). it was in the Sea of Okhotsk that Ushakov, then on board the

trawler "Gagara", recovered the first-ever animal specimen from a depth of more than 3,000 m. Among them were

hitherto unknown animals for which the new phylum Pogonophora was later erected.

Based on the study of flora and fauna of the Sea of Okhotsk he suggested for the first time a scheme of vertical

zonation of the sea and showed that tire Sea of Okhotsk and die Pacific Ocean were connected at depth via the

straits between the islands making up die Kuril Island Arc.

In 1931, he organized Kamchatka Marine Station in Avachinskaya Bay. In 1933, he received the degree of

Doctor of Biological Sciences. From 1936 to 1939, he organized Murmansk Biological Station of the USSR

Academy of Sciences in Dalniye Zelentsy and developed investigations there. In 1939, he returned to the State

Hydrological Institute. He supervised and participated in preparing hydrological manuals on the Okhotsk and

Bering seas. During World War II, P.V. Ushakov was in military service in the rank of engineer major and

worked on hydrometeorological manuals for die Navy.

From 1946 to 1982 P.V. Ushakov worked at the Zoological Institute of the USSR Academy of Sciences

(Leningrad). He was die head of the Laboratory of Marine Research of die Institute until 1966. Then he became

Curator of the Department of Annelids and Bryozoans. At that period, he focused on marine fauna, ecology and

biogeography, systematics and phylogeny of polychaetes. In 1948, he participated in die Kuril-Sakhalin expedition

of the Zoological Institute and Pacific Institute of Fisheries and Oceanography on board the "Toporok" research

vessel. Material of this expedition formed an important part of his book "Polychaetes of the Far Eastern Seas of

die USSR" (1955). In 1949, he took part in the first Pacific voyage of the "Vitiaz" research vessel and conducted

trawling in the Kuril -Kamchatka trench, when bottom-dwelling animals were recovered from a depdi of more than

8,000 m for the first time. In 1950 he published "Polychaetes of the Sea of Okhotsk". In 1956, he participated in

the first Soviet Antarctic Expedition on the research vessel "Ob". As a result of the expedition, he published a

number of papers dealing widi quantitative distribution of benthos in Antarctic waters, patterns of vertical

distribution of biocoenoses of bottom fauna and widi systematics of Antarctic polychaetes. In 1957 and 1958, he

worked on the Yellow and South China seas. In 1963, he conducted biological studies in Gulf of Guinea.

P.V. Ushakov visited France several times where he lectured in Marseilles University and in Sorbonne (Paris

University). In 1965, he published "Polychaeta Errantia of the Yellow Sea" widi Wu Baoling. In 1972, he

published his monograph "Polychaetes of the suborder Phyllodociformia of die Polar Basin and die nordi-western

part of die Pacific" and in 1982 "Polychaetes of the suborder Aphroditiformia of die Arctic Ocean and the north¬

western part of the Pacific".

During the last 10 years P.V. USHAKOV lived in Pushkkin town in die House of Science Veterans where he

wrote papers and essays on the history of science, memoirs about fellow scientists, i.e., his friends and

contemporaries. His colleagues and disciples visited him regularly to discuss widi him results of their studies and

new initiatives.

Everyone who was fortunate enough to work and meet widi P.V. Ushakov will keep fond memories of him.

Source :

OBITUARIES

21

Some personal souvenirs of P.V. USHAKOV

Lucien LAUBIER

Institut Oceanographique

195, rue Saint- Jacques

75005 Paris, France

Since the Long Beach Conference, some famous polychaetologists have disappeared. Among others, I am

thinking of Professor David Dean, Professor Pavel Vladimirovitch Ushakov and Professor Douglas P. Wilson.

The death of P.V. Ushakov, at the beginning of this year, was particularly sad for me and I would like to recall

with his friends and colleagues a few souvenirs of the different visits he made in France.

I first met P.V. Uskhakov in Summer 1965. Me came from Marseilles to my laboratory in Banyuls-sur-Mer

and spent a few days there. I remember a one day trip to the Spanish boarder, at a small village called Le Pcrthus.

P.V. Ushakov was astonished to discover that he, a citizen from die USSR, could walk through the custom

freely, from France to Spain and back, without any inquiry from the french and Spanish guards. On die same day.

P.V. Ushakov experienced the french way of eating snails, and found them just delicious. At the end of this

visit, I took him with my car from Banyuls-sur-Mer to Angers: I had a radier fast car, a Citroen DS 19, and speed

limitations were not a major problem for me. P.V. Ushakov remained very quiet at 100 miles per hour, but I

found later on that this journey became one of his frequent story when speaking of our relationship with other

people ! W'e reached Angers without any uouble, and P.V. Ushakov worked a few days with Francois RULLIER.

When die Second Oceanographic Congress took place in Moscow, in 1966, 1 attended the Congress and I had

the opportunity to make a one day trip in Leningrad, now Saint Petersburg. P.V. Ushakov invited me with

Professor M. FONTAINE for a tea party in his small flat, where he lived widi his daughter in law.

P.V. Ushakov came back to Banyuls-sur-Mer in die Winter 1967-68, and spent a full fortnight working on

Mediterranean Polychaetes. We went at sea togcdicr on board die small trawler Nereis, and P.V. Ushakov was

specially interested by a one meter long Eunice rousseaui living in a special glass-tube whick I kept for more dian

six years in my laboratory and exhibited during the easter and summer courses to die students. The regular wave

along the body of die movement of the pectinate branchiae was fascinating... P.V. Ushakov asked me for a

posterior part of die worm, which I knew regenerated easily, and I gave him some 300 segments of diis large

Mediterranean Eunice which quickly recovered. During that visit, we had a party in my flat for Christmas night:

we were all very surprised when P.V. Ushakov quietly asked us about midnight Christmas mass: do French

people usually go to church for Christmas mass? Moreover, he decided he wanted to go to church himself, where

he attended the whole office.

When 1 moved to Brest, beginning of 1969. It was more difficult to Wellcome P.V. Ushakov in my next

laboratory, due to die fact that Brest is also our main naval base for nuclear submarines... Nevertheless, I obtained

that P.V. Ushakov could come for two days under special permission. We had a long discussion about the 1917

Revolution, and P.V. Ushakov told me that he very clearly saw the shots of the cruiser Aurora of die Winter

Palace in Leningrad. At that time, I was working on deep-sea Mediterranean Polychaetes collected in the Hellenic

Trench. I was specially interested by an aberrant tiny worm combining spiomorph and tercbellomorph features.

P.V. Ushakov agreed on die fact diat it should be described as a new genus. In fact, I described it its Ushakovius

enigmaticus , type of a new sub-family, and Professor M. Fontaine told P.V. Ushakov of diis new child when

he gave to Professor Ushakov the Manlay-Bendall medal of die Institut Oceanographique in Paris, a few weeks

after his visit to Brest. A few days later, P.V. Ushakov told me diat it should constitute a new family, which in

fact was recently proposed by B. Molte.

Later on, P.V. Ushakov retired from the Zoological Institute, I had no more opportunity to visit USSR, and

I received some news exchanging letters with him. Me of course wrote in French. Finally, Marina Dolgolenko

was our last link.

I am sure all those who have had the chance to met P.V. Ushakov and experienced his happiness will share

my deep sadness.

22

OBITUARIES

Douglas P. WILSON

1902-1991

David GEORGE

Department of Zoology

Natural History Museum

Cromwell Road

London, SW7 5BD. Royaume Uni

Dr. Douglas P. Wilson died suddenly on 18 December 1991 aged 89. "DP", as he colleagues, was born in

Manchester and educated at William Hulme's Grammar School. After leaving school he started on a career in the

Lancashire cotton industry, but this career was cut short by a dramatic slump in the cotton trade. Having from a

very early age been keenly interested in natural history (particularly aquatic life) he decided to attend evening

classes in zoology at Manchester University and also joined the Manchester Microscopical Society. This led to

him doing practical work on die shore and to a decision that a career in zoology offered him a better life than a

career in business. Consequently he enrolled in 1923 on a BSc course in zoology at Manchester University during

which time he attended marine biology courses at Millport, Port Erin and Plymouth. Having gained a first class

degree he obtained a grant in September 1926 to study polychaete development at die Marine Biological

Association's laboratory at Plymouth, where less than a year and a half later, he was appointed to die staff as

Assistant Naturalist widi special responsibility for development of the public aquarium. DP remained at this

marine station for die rest of his working life, officially over 10 years as Deputy Director, aldiough continuing to

work diere until the end of 1981. From die start of his career at die laboratory until die beginning of the second

world war. D.P. studied in detail die early development of polychaetes of many different families. His ability to

rear polychaete larvae in die laboratory combined widi his skills as a microscopist and a keen eye for detail

contributed in no small measure to the scientific accuracy of his early research publications.

During die 1930's he began to investigate the influence of die substratum on die metamorphosis of larvae of

such species as Scolecolepis fuliginosa and Noiomastus latericeus, but unfortunately the war years and more

applied research intervened. The Plymoudi laboratory had cause to be grateful to DP during die second world war

because it was his team of fire-fighters that saved die majority of die building by putting out die fires started by

incendiary bombs dropped during an air raid.

After the war he returned to his work on habitat selection by metamorphosing larvae and produced a series of

papers using mainly Ophelia bicornis as his experimental animal. He was able to show that larval settlement

could be delayed for some considerable lime if die substratum was not suitable, and that micro-organisms played

an important role in making die substratum attractive to larvae. In 1951 he was awarded the Prix George KOHN,

an award of the Institut Oceanographique, Paris for a summary paper on this research. I Ic had by diis time obtained

his DSc from Manchester University for his investigations on die early development of polychaetes.

In parallel with this work, and continuing until the late 1950’s, DP conducted an interesting series of

experiments on die "quality" of seawater in collaboration with a chemist at die laboratory, F.A.J. Armstrong.

Using sea urchin larvae he was able to show dial larval development took place at different speeds and with

varying degrees of success in seawater from different areas. In effect he had discovered a biological method for

distinguishing seawaters of different origins, which effectively complemented die plankton indicator species

concept developed by colleagues at the laboratory.

He next turned his attention to die biology of British species of magelonid and in die process uncovered some

taxonomic problems which he solved by erecting two new Magelona species in the late 1950’s. Interestingly his

last scientific publication in 1982 returned once again to die genus, describing die larval development of three

species from Idealities near Plymouth and Salcombe. However, most of DP’s later contributions to the study of

polychaetes dealt with British species of the Sabellariidae, the larvae of which he described in one of his earliest

papers in 1929.

Soon after he recommenced work on die sabellariids die “Torrey Canyon” oil-tanker disaster occurred and he

was able to use larvae of Sabellaria spinulosa to assess die long-term effects of low concentrations of die detergent

used to clean up the oil. He followed this by studies on die early development of the reef-building shore-dwelling

honeycomb worm Sabellaria alveolaia and combined the laboratory work widi valuable long-term monitoring of

Source :

OBITUARIES

23

recruitment and succession in colonics of the worm at Duckpool in north Cornwall from the early 1960's through

lo the mid 1970's. He showed that die larvae could delay metmorphosis, sometimes for many weeks, until a

suitable substratum was found, and dial they settled in preference on or near tubes of die same species, being

attracted primarily by the chemical composition of the cement binding die sand grains of die tubes together.

During diese studies he made extensive use of photography to record not only die morphology of the developing

larvae but also die changes in die shore colonies with time.

FlG. 1. Professor Douglas P. WILSON

Source :

24

OBITUARIES

From an early age DP had been interested in the art of photography and he was a pioneer in the photography of

living marine animals on the shore, in tanks, and under the microscope. Indeed, he was almost certainly the first to

adapt electronic flash for the photography of living planktonic organisms, his dark-field photomicrographs being

particularly impressive, even today. It was for his pioneering work in this field that he received an honorary

fellowship of the Royal Photographic Society in 1987.

As well as being remembered by those with a special interest in polychaetes and marine life photography, DP

will be remembered by the many hundreds of students who attended die famous caster vacation courses in marine

biology at the Plymouth laboratory, for it was he who was the principal organizer of these between 1930 and

1948. Neither will his skills as a popular author be forgotten by those who have copies of "Life of the shore and

shallow sea" and "They live in the sea".

Source : MNHN. Paris

CONTRIBUTED PAPERS

Cytophysiology, development and reproduction

1. Evolution of viviparity in the genus Ophryotrocha (Polychaeta, Dorvilleidae) 2 9

Bertil AkeSSON

2. Environmental influences on endocrine systems controlling reproduction

in Polychaetes 3 7

Matthew G. BENTLEY, Jcni BOYLE & Allan A. PACLEY

3. Morphometric analysis of cellular specification in Platy nereis and Pomatoceros

embryogenesis (Annelida, Polychaeta) 4 5

Adriaan W.C. Dorresteijn & Craig Marc LUETJENS

4. Observations on reproduction and growth of Sahella spallanzanii (Polychaeta,

Sabellidae) in the Mediterranean Sea 5 1

Adriana GlANGRANDE & Angela Petrarou

5. The functional significance plexuses in the ecology of Ophelia hicornis Savigny 5 7

Tegwyn Harris

6. Feed-back regulation in Platynereis dumerilii Audouin & Milne-Edwards, 1833:

a status review 6 5

Dietrich K. HOFMANN

7. Bioaccumulation du fer dans lc corps cardiaque de Karicirrus heryli

Petersen & George (Polychaeta, Ctenodrilidae) 7 3

Jean VovELLE, Mary E. PETERSEN. Michele GRASSET & Patricia BEAUNIER

Genetics and morphology

8. Functional ciliary groups of the feeding palps of Spionid polychaetes 8 1

Daniel M. DaUER

9. Attributes of ribosomal DNA in alvinellid polychaetes from hydrothermal vents 8 5

David R. DIXON, Linda R.J. DIXON & Verena TUNNICLIFFE

10. On the nature of the two anterior asetigerous rings in Dorvilleidae and

Dinophilidae (Annelida, Polychaeta) 9 3

Danny Eibye-Jacobsen

11. The head of Maldanidae polychaetes of the subfamily Maldanidae 101

Karen D. GREEN

12. Effects of sample fixation on body shape of Capitella capitata

(Polychaeta, Capitellidae) 1 1 1

Maria Nuria MENDEZ & Maria Jose CaRDELL

13. infrastructure of sense organs and the central nervous system in

Parenterodrilus taenioides and their phylogenetic significance in the

taxon Protodrilida (Annelida, Polychaeta) 119

Gunter PURSCHKE & Claude JOUIN-TOULMOND

14. Genome size in Polychaetes: relationship with body length and life habit 129

R. Soldi. L. Ramella. M. Cristina Gambi, Paolo Sordino & Gabriella Sella

Source :

26

CONTRIBUTED PAPERS - CONTRIBUTIONS

15. Fine morphology of the feeding apparatus of Cossura sp. (Polychaeta,

Cossuridae) from the White Sea 1 3 7

Alexander B.TZETLIN

Phytogeny and taxonomy

16. Polvchaetes of the family Acoetidae (= Polyodontidae) from the Levant and the

Central Mediterranean with a description of a new species of Eupanthalis 145

M. Nechana Ben-Euahu & Dieter FlEGE

17. Prionospio caspersi Laubier (Polychaeta, Spionidae) in the Black Sea:

long-term monitoring of a population 163

Temir A. Britayev. Alberto CASTELLI & Tatiana S. AKSIUK

18. Systematics, ecology and biogeographic relationships in the sub-family

Travlsiinae (Polychaeta, Opheliidae) 169

Jean-Claude Dauvin & Gerard Bellan

19. A new' species of Ophryothrocha (Polychaeta, Dorvilleidae) associated with

ice scours in the Canadian Arctic Archipelago 185

Judith A. FOURNIER & Kathleen E. CONLAN

20. Two new species of Branchiomma (Sabellidac) with rcdcscriptions of closely

related species and comments on Pseudobranchiomma and Sabellastarte 19 1

Phyllis Knight -Jones

21. Redescription of Hipponoa gaudichaudi Audouin & Milne-Edwards, 1830

(Polychaeta, Amphinomidae) 199

Jerry D. KUDENOV

22. Sabellariidae (Annelida, Polychaeta) from south America 2 09

Paulo da Cunha Lana & Claudia Silvia BREMEC

23. The phylogenetic position of the Pilargiidae with a cladistic analysis

of the taxon - facts and ideas 22 3

Frank LlCHER & Wilfried Westheide

24. Pseudatherospio fouchaldi a new genus and species of Spionidae

(Polychaeta, Annelida) from the Southern California, USA 23 7

Laurence L. Lovell

25. Adercodon pleijeli gen. and sp. nov. (Polychaeta, Ampharetidac) from the

Mediterranean Sea 24 1

Andrew S.Y. Mackie

26. The genus Ophryotrocha sensu Into (Polychaeta, Dorvilleidae) in the Tromso

area, Northern Norway 2 5 1

Eivind OUG

27. Distributional patterns and taxonomic notes on Lumbrineridae from Crete

(S. Aegean, eastern Mediterranean) 2 59

K. Nadia Papadopoulou, C. DOUNAS & Chris J. SMITH

28. Autolytinac (Polychaeta, Syllidae) from Cuba and north American Atlantic Ocean 2 69

Guillermo SAN MARTIN

29. New arctic species of Scolelepis (Polychaeta, Spionidae) 279

Andrew V. SlKORSKI

30. A systematic problem of inter- and intra-generic variation in nephromixia

of Terebellidae 2 87

Ralph 1. Smith

31. Morphometric variation in bifurcate notosetae of two Euphrosine species

(Polychaete, Euphrosinidac) 29 1

Ken D. Vogt & Jerry D. KUDENOV

Source :

CONTRIBUTED PAPERS - CONTRIBUTIONS

32. Pseudonotomastus southern! gen. nov., a new capitellid from the Celtic Sea 2 99

Lynda M. WARREN & Miles PARKER

33. A new species of Chaetozone (Polychaeta, Cirratulidae) from Europe,

with a redescription of Caulleriella zctlandica (McIntosh) 307

Annette WOODHAM & Susan CHAMBERS

34. Phylogcny of Alciopidae (pelagic polychaetes): a cladistic analysis 3 1 7

Baoling Wu & Lua Hua

Ecology and biogeography

35. Preliminary observations on a dense population of Plyllochaetopterus socialis

Claparede at the sulphurous water boundary in a Mediterranean submarine cave 3 23

Marco ABBIATI, L. AlROLDI, Alberto CaSTELLI, F. ClNELLI & AJ. SOUTHWARD

36. Contribution of the Polychaetous annelids to the diet of some brazilian fishes 33 1

A. Cecil ia Z. AMARAL. Edmundo F. NONATO & Monica A.V. PETTI

37. Ecology of Pherusa sp. (Polychaeta, Flabelligeridae) 33 9

Analfa AMOR

38. Polychaete fauna associated with the coral Cladocora caespitosa (L.)

in the eastern Mediterranean 34 7

Christos ARVaNITIDIS & Athanasios KOUKOURAS

39. Morphology, ecology, and juvenile development of Cossura pygodactylata

Jones (Polychaeta, Cossuridae) in Arcachon Bay, SW France, with a reassessment

of the geographic distribution of C. pygodactylata and C. soyeri Laubier 3 55

Guy BaCHELFT & Lucien LAUBIER

40. Larvae-substrate relationships of Eupolymnia nebulosa (Montagu, 1818)

(Polychaeta, Terebcllidac): an experimental analysis 37 1

Michel Biiaud & Jae H. Cha

41. Is Owenia fusiformis a cosmopolitan species? 3 83

Jean-Claude DaUVIN & Eric ThiEbaUT

42. Light influence on larval emission and vertical swimming in the terebellid

worm Eupolymnia nebulosa (Montagu, 1818) 4 05

Jean-Claude DUCH&NE & Christian Nozais

43. Polychaeta of the German Bight from the 1987 cruise of the R/V "Senckenberg" 4 13

Dieter FlEGE & Nechama BEN-ELIAHU

44. Selection des grains de sable selon leur nature et leur forme par

Sabe/laria alveolata Linne (Polvchete, Sabellariide) lors de

la reconstruction experinientale de son tube 4 25

Yves GRUET & Yves BODEUR

45. Les vers polychetes et l'estuaire de la Loire au debut du 20eme siecle

par G. FERRONNIERE (1875-1922) 433

Yves GRUET, Joceiyne March and & Joseph Baudft

46. Temporal and spatial patterns in the distribution of infauna] polychaetes

in Jervis Bay, New South Wales, Australia 44 1

Patricia HUTCHINGS & C.A. JACOBY

47. Ecology and biogeochemistry of an Paralvinella sulf incola at

northeast Pacific hydrothermal vents: review and comparison with

A /vine l la spp. of the east Pacific rise 4 53

S. Kim Juniper

48. Polychaete assemblages along a depth gradient in a Spitzbergen Fjord 4 63

Michael A. KENDALL

49. The biogeography of some abyssal polychaetes 47 1

J0rgen B. KirkegaaRD

28

CONTRIBUTED PAPERS - C'ONTRIBUTIONS

50. Preliminary results on recolonization in a small brackish basin on the

island of Elba (western Mediterranean)

Claudio Lardicci & R. Baldi

51. Intertidal sandy beaches polychaetcs of Sao Sebastiao island, Southern Brazil

Eloisa H. Morgado. A. Cecilia Z. Amaral, Edmundo F. Nonato & Lara B. Salvador

52. Influence of the tube-building spionid polychaete Polydora ciliata on

benthic parameters, associated fauna and transport processes

Carol a Use-Marie NOJI

53. Patterns of abundance and diversity from the abyss - Polychaetcs from

northeastern Atlantic abyssal plains

Gordon L.J. Paterson. John D. Gage. P. Lamont. B.J. Be tt & M.T. Thurston

54. Polychaete response to different aquaculture activities

Patricia POCKUNGTON. David B. SCOTT & C.T. SCHAFER

55. Influence of temperature and diet on the larval development and growth

of juveniles Marphysa sanguined (Montagu) (Polychaeta, Eunicidae)

Daniela Prevedelli

56. Ethologie alimentaire d'Annelides Polvchetes endogees : determination

du niveau sedimentairc oil s'effectue la collecte de nourriture

Chantal SalEN-PicaRD, Claire Graham & Magali GERINO

57. Polychaete distribution patterns on Chlamys palagonica of the Magellan Strait

Rossana SANFILIPPO

58. Polychaeta in the cstuarv of the Piaui River, Sergipe, Brazil

Maria A. Santos. C.S.G. Santos & C.M.M. Oliveira

59. Life history of the polychaete Polydora variegata that bores into the shells

of scallops in Northern Japan

Waka Sato-Okoshj

60. Annelid polychaete populations of the Order Eunicida from the southern

Gulf of Mexico

Vivianne Solis-Weiss, Luz Veronica Rodriguez-Viixanueva, Alejandro Granadas-Barba.

Victor Ochoa-Rivera. Luis Miranda-Vazquez & Pablo II ernant>ez- Alcantara

61. Ecological analysis of some Syllidae (Annelida, Polychaeta) from

the central Tyrrhenian Sea (Ponza Island)

Alessandra SOMASCHLM & Flavia Gravina

62. Cyclical changes in the fauna associated with tube aggregates of Ficopomatus

enigmatic us (Fauvel)

Nigel S. Thomas & Clifford IT Thorp

63. Population variation in Ficopomatus enigmaticus (Fauvel) (Polychaeta,

Serpulidae) in a brackish water millpond at Emsworth, West Sussex, U.K.

Clifford H. Thorp

Culture and valorisation

64. Polychaetcs of commercial and applied interest in Italy: an overview

M. Christina Gambi. Alberto CASTELLI. Adriana GlANGRANDE, Daniela PREVEDELLI &

R. ZUNARELLI VaNDINI

65. Polychaeta as a world resource: a review of patterns of exploitation

as sea angling baits, and the potential for aquaculture based production

Peter J.W. Olive

479

4 85

493

503

5 1 1

52 1

527

53 5

5 4 1

54 9

559

567

575

585

5 93

6 03

Source : MNHN. Paris

1

Evolution of viviparity in the genus

Ophryotrocha (Polyehaeta, Dorvilleidae)

Bertil AKESSON

Department of Zoology

University of Goteborg

Medicinaregatan 18

$-413 90 Goteborg. Sweden

ABSTRACT

Brooding is a common feature in the genus Ophryotrocha. Viviparity, the most extreme type of parental care, is

represented by only one species, O. vivipara , but tendencies towards viviparity have also been reported from gonochoric as

w'ell as hermaphroditic species. Except for the viviparous species, all species studied deposit their eggs in a gelatinous matrix.

The surface of the egg mass may remain soft and sticky, but in two distinct species groups the surface hardens to a solid

membrane that encloses gel and eggs. In both groups newly spawned egg masses may occasionally contain a few young larvae.

Such larvae never occur in a young female’s first egg mass. The larvae arc interpreted as originating from fertilized eggs that

have been trapped in the coelom of the female during a previous spawning. They develop inside the female at a retarded rate.

In O. socialis not only lar vae at an early stage of development are released but also larvae/juveniles at more advanced

stages. Usually they are released together with a normal spawn, but they may also appear single. Juveniles with up to 12

setigerous segments have been observed. During the normal course of development, the 12-setiger stage is attained after about

80 days. At that age they have already developing oocytes in the coelom whereas the viviparous progeny with the same number

of segments have not.

Observations of incipient viviparity in three species groups call for a reevaluation of some previous reports on self-

fertilization and on viable larvae obtained in crosses between species that are otherwise reproductively isolated.

RESUME

Evolution dc la viviparite dans le genre Ophryotrocha (Polyehaeta, Dorvilleidae)

C’est un tr ait frequent du genre Opluyotrocha d’incuber ses oeufs. La viviparite, le type le plus extreme du soin parental, est

representee chez une espece, O. vivipara . mais des tendances vers la viviparite out aussi (Ste rapportees chez des especes

gonochoriques aussi bien que chez des especes hermaphrodites. Exception faite des especes vivipares, toutes les especes

etudiees deposent leurs oeufs dans une matrice gelalineuse. La surface de la masse d’oeufs peut rester molle et collante. mais

dans deux groupes d’especes distincts. cette surface durcit en une membrane solide qui renferme le gel et les oeufs. Dans les

deux groupes. des masses d’oeufs recemment deposecs peuvent conlenir, de temps en temps, quelques rares larves/juveniles.

De telles larves n’apparaissent jamais dans la premiere masse d’oeufs d’une jcunc fcmclle. Les larves proviennent probablemcnt

d’oeufs fecondes anterieurement qui sont restes dans le coelome de la femelle ou ils se sonl developpes lentement.

Chez O. socialis des individus larve/juvenile. h un stade avance sont relaches en meme temps que des larves en debut de

developpement. Habituellement elles sont emises en meme temps qu’une ponte norinale, mais elles peuvent aussi apparaitre

AKESSON. B.. 1994. — Evolution of viviparity in the genus Ophryotrocha (Polyehaeta. Dorvilleidae). In: J.-C. Dauvin.

L. Laubihr & D.J. Reish (Eds). Actes de la 4eme Conference internationale des Polychetes. Mem. Mus. natn. Hist, nat., 162 :

29-35. Paris ISBN 2-85653-214-4.

Source . MNHN. Paris

30

B. Akesson

sculcs. Dc tcls juveniles ayant jusqu’a 12 segments sctigeres ont etc observes. Au cours d'un developpcment normal ce stade 12

setigeres n’cst atteint qu'apres environ 80 jours. Ces larves/juveniles ont alors deja developpe dcs ovocytes dans le coelome

Landis qu'il n’y a pas d’ovocytes dans les juveniles issus d'un developpcment vivipare au mcme stade de devcloppement. Les

observations failes sur cette tendance a la viviparite dans les 3 groupes d’especes nous conduisent a une revision des resultats

anterieurs traitant de l'autofecondation et aussi des larves viables qui en realite n'ont pas ete obtenues dans des croisements

enlre especes differences.

INTRODUCTION

Brood protection has evolved many times among boll) invertebrates and vertebrates (Hogarth, 1976;

Clutton-Brock. 1991). The same applies also to viviparity, the most extreme form of brood protection.

Evidence from most groups indicates that viviparity has evolved from oviparous ancestors and that internal

fertilization has been a preadaptation for the evolution of viviparity. In transition stages fertilized eggs have been

retained for progressively longer periods of time. They do not receive any nutrients from the female and tliis holds

true also for species with ovoviviparity, the least advanced form of viviparity. In more advanced viviparous forms,

the female continues to provide the embryos with nutrients. Often a kind of placenta analogue develops or the

embryo/larva receives nutrients from surrounding body fluids of the female.

For the evolution of viviparity from oviparous ancestors to occur, transition stages must also be selected. The

continuing discussion has been widened to involve other aspects of brood protection and its relation to egg size.

Shine (1978) suggested the "safe harbor" hypothesis according to which optimal offspring size is determined by

relative mortality rates of egg stages and free-living juveniles. Selective forces tend to maximize die time spent in

the safest stages of development. In brooders eggs are safer than juveniles which should account for die positive

correlation often seen between brood protection and large egg size (Shine, 1989; Clutton-Brock, 1991).

According to Hogarth (1976), evolution towards viviparity is favoured in species that already produce a

restricted number of eggs. Retention and viviparity protect die progeny against bodi predators and harsh

environmental conditions such as cold climate, desiccation or, for marine animals, suboptimal salinity levels.

Viviparity has been reported from several polychaete families and SCHROEDER & Hermans (1975) have listed

19 species. I lowever, for 9 of these the original reports on viviparity have not been verified in later studies. Many

older reports on viviparity were analyzed by Smith (1950) who provided evidence dial some of them were

erroneous. Some embryos or larvae from inside the body of polychaetes were either developmental stages of

parasitic polychaetes or turbellarians.

The purpose of diis paper is to describe a possible line of evolution towards viviparity in the genus

Opliiyoiroclia of the family Dorvilleidac. Dorvilleid polychaetes arc generally small and many of the smallest,

nonpar aside species belong to the genus Opliiyoiroclia. Only direc species exceed a lengdi of 10 mm. Two of

these are commensals in the gill chamber of crabs (Martin el al. , 1991), die third one is found near geothermal

vents (Blake, 1985). The smallest of all Opliiyoiroclia species, 0. vivipara Banse, 1963, is only 0.8-1 mm long.

Banse's description was based on two specimens from die vicinity of Friday Harbor, Washington. This was the

only record until I collected about 50 specimens in the aquarium of the Tjarno marinbiologiska laboratorium

located about 200 km north of Gothenburg. Opliiyoiroclia vivipara is one of the few species that I have failed to

maintain as a laboratory culture; nondieless Banse's observation of a truly viviparous species could be confirmed.

The juveniles have two or three setigerous segments when released from the posterior end of die female.In contrast

to a uniform adult morphology in most species, reproduction is remarkably variable. In addition to the traits listed

m I able 1. species or species groups may also vary in odier reproductive adaptations such as clutch size and time

between consecudve spawnings, sex ratio in gonochoric species and amount of energy allocated to individual egos

(Akesson, 1973).

Mating behaviour is equally variable. Sella (1985. 1988) analyzed pair formation and egg hading in the

simultaneous hermaphrodite O. diadema. A behaviour has evolved that safeguards against non-reciprocating

partners. In gonochoric species, females often discriminate against males from other geographic populations and

they certainly do so in interspecific crosses (AKESSON, 1972a, 1977b. 1978, 1984). In the protandrous

hermaphrodite O. puerilis, sex reversal may occur several limes in the same individual. In pair cultures with

females, the result ol lights over sex will be that the winner remains female and the loser changes to male

BERG LUND ( 1991) has shown that females prefer small mal es. If a female mates widi a large male, she is at risk of

being challenged to change sex when she is weakened after spawning.

Source :

EVOLUTION OF VIVIPARITY IN THE GENUS OPHRYOTROCHA

31

Table 1. — Reproductive traits in the genus Ophryoirocha.

Incipient viviparity has been reported from the simultaneous hermaphrodite 0. diadema (Akesson. 1973,

1976). Occasionally one or two larvae appear in newly spawned egg masses, but never in a female's first brood.

The fusiform egg masses of 0. diadema are surrounded by a tough wall and larvae cannot enter an egg mass from

the outside.

As in all other known Ophryoirocha species, fertilization in 0. diadema is preceded by a kind of

pseudocopulation similar to that described by Westheide from 0. gracilis (Whstheide, 1984, fig. 3). Selling has

not been observed. Eggs and spermatozoa arc shed into a gelatinous matrix and mingle there. 'The egg mass is

molded to its final shape and usually attached to a substratum. 'Then the surface of the mucus hardens to form the

lough outer wall.

The explanation suggested for the presence of larvae in newly spawned egg masses is that a few eggs have

been trapped in the female part of the coelom during a previous spawning. They have been fertilized by entering

spermatozoa, developed inside the body, and then released together with die next spawn (Akesson, 1976).

The same type of incipient viviparity as in O. diadema has also been observed in several members of the

labronica group, a group of related gonochoric species within the genus (Akesson, 1973). Members of that group

produce a different kind of egg mass that is tube-shaped and contains smaller, but more numerous eggs than that of

0. diadema. Enclosed larvae inside newly spawned egg masses have been observed in 0. labronica ,

0. nologlandidata , and 0. macrovifera , and they may occur in all members of the labronica group.

Ophryoirocha socialis , another simultaneous hermaphrodite, was recently described by OCKELMANN &

Akesson (1989). The gelatinous matrix around the eggs is sparse in this species but there is enough to attach the

eggs to each other forming tubular or irregular egg masses. As in 0. diadema fertilization lakes place after

pseudocopulation. Isolated individuals may self- fertilize but such self-fertilization is external.

In a still ongoing life table study that began with fertilized eggs, O-setiger larvae occasionally appeared in the

bowls when the experiment had continued for about 6 months. The larvae were at die stage of development that is

normally obtained in 3 weeks (OCKELMANN & Akesson, 1989, Fig. 10). Since the adult worms were transferred to

clean bowls once a week, these larvae could not be die result of a previous spawn. Eventually more advanced

larvae could also be collected, i.e., larvae with 1-2 or more setigerous segments. The peak production of such

larvae was observed when the adults were 10 months old and had 19-20 setigerous segments. In one week 40

adults had produced 1 1 0-setiger larvae

Source :

32

B. Akesson

and 17 juveniles with 7-12 setigers (mean 9.9 ± 0.4). In addition, die adults had spawned 919 eggs during the

same week.

After a normal spawning, die progeny develops into functional males with 6 setigers after about 50 days. The

first spawning was observed at an age of 60 days in worms with 10 setigers. Only few worms spawn before the 11-

sedgcr stage (Ockelmann & Akesson, 1989). Not even the largest viviparous progeny had any visible oocytes in

the coelom. They were more slender than larvae widi the same number of setigers that develop after normal

spawning. It has not been possible to determine the age of die viviparous progeny when released from the coelom.

REEVALUATION OF SOME PREVIOUS REPORTS

The observations of incipient viviparity in two species groups as well as mixed oviparity and viviparity in 0.

social is may justify a reevaluation of some previous reports on self-fertilization and on results of crossing

experiments.

Hartmann (1943) and Bacci (1978) reported on rare instances of self-fertilization in 0. puerilis. In some

crosses between die Adamic and Mediterranean subspecies of 0. puerilis, a very low percentage of spawned eggs

were reported to develop into viable larvae (Akesson, 197.3). The possibility should be considered dial these

reports concern incipient viviparity of the same kind as in 0. diadema and the labronica group. However, it is

evident diat some species may reproduce by both cross-fertilization and self-fertilization. This is true of 0.

labronica ( but note die discussion about identity of species in Akesson, 1984), 0. socialis, and a not yet

described species from Florida (La Greca & Bacci, 1962; PaRENTI,1960; Zunarelli, 1962; Zunarelli-

Vandini, 1967; Akesson. 1984; Ockelmann & Akesson, 1989).

In the light of these findings, die previous report on partial success in crosses between die Pacific species 0.

notoglandulala and 0. labronica pacifica should be reevaluated. Akesson (1984) reported dial occasionally a few

(< 10) viable hybrids were obtained in crosses between female O. noioglandulata and male O. I. pacifica. These

supposed hybrids were all female and therefore IA hybrid breakdown could not be tested. No progeny was

obtained in backcross with O. I. labronica males except for a few larvae. As in die first cross, the number of larvae

per egg mass was always below 10. In backcross with O. noioglandulata many egg masses were produced, usually

widi almost 100 % development.

A return to die original data sheets revealed that in the interspecific cross only 5 "hybrids" developed into

normal, mature females. They were first used in backcross widi male O. noioglandulata and then with O. I.

labronica. Previous and subsequent crosses between O. labronica (both subspecies) and 0. noioglandulata proved

to be intersterile. More than 100 egg masses in each reciprocal cross have been observed. Moreover, die "hybrid"

progeny reported by Akesson (1984) was all female. The same was true of all viviparous progeny observed so far

in die diree gonochoric species where incipient viviparity has been recorded. A very likely explanation of die

crossing results (Akesson, 1984) is dial the few larvae obtained were an expression of incipient viviparity.

In recent experiments widi both inter- and intraspecific crosses, individual egg masses have been analyzed for

enclosed larvae. Such larvae are found in less dian 5 % of the egg masses and' only in egg masses produced by

females diat have spawned previously. The fact diat such larvae were produced in two subsequent generations in

the crosses reported by Akesson (1984) may indicate a heritability of die trait, but recent selection experiments

with viviparous progeny has not yet proved diis.

DISCUSSION

For the evolution of viviparity in die genus Ophryotrocha, transition stages between oviparity and viviparity

should have a selective advantage. One such advantage may be dial those embryos that are retained in the female's

body have better chances of survival than die siblings which are fertilized and spawned at the same time. A

brooding worm presumably has better chance of escaping a predator than embryos enclosed in an immobile egg

mass that die female will desert when attacked.

Internal fertilization as a prerequisite for viviparity is not fulfilled in Ophryotrocha, but functionally die kind of

pseudocopulation found in die genus comes close to internal fertilization (WESTHE1DE. 1984). The final stage,

obligate viviparity, is found in the smallest known Ophryotrocha species only. This may be an indication that die

evolution of viviparity is one of many adaptations to 'the problem of being small'. As has been repeatedly

discussed for meiofauna species (Swedmark, 1964; WESTHEIDE, 1984), smaller size is correlated widi changes in

Source : MNHN. Paris

EVOLU TION OF VIVIPARITY IN THE GENUS OPHRYOTROCHA

33

reproductive traits compared to related larger species. WESTHEIDE (1987) demonstrated how progenetic (neotenic)

evolution has been one of the major forces behind adaptation to die interstitial habitat. The morphology of an adult

Ophryotrocha is very similar to the larval morphology of larger cunicid polychaetes, e.g., to the larvae of

Dorvillea rudolphi (Richards, 1967). The evolution of progenesis is also demonstrated in Westheide’s (1987)

series of increasingly juvenile characters in dorvilleid genera where die endpoint is die dinophilid genus

Dinophilus. It has been shown dial dinophilids are closely related to cunicids (Hermans, 1969; Akesson. 1977a;

WESTHEIDE, 1985).

Reproduction in the genus Ophryotrocha is more variable than in any other polychactc taxon of similar size.

Energetic constraints related to small size may be one reason; opportunistic life histories widi often sparse

populations may be another. The most important of those reproduclive traits are listed in Table 1.

WESTHEIDE's (1987) series of successive embryonization in die family Dorvilleidac indicates dial small species

have evolved from larger ones, —"these small interstitial species must then form die end-point of an evolutionary

line which originates in larger benthic species" (WESTHEIDE, 1984, p 266). For die genus Ophryotrocha it has also

been suggested that the alrochal, demersal larvae found in 0. maculata occurred in die larger ancestors

(Zavarzina & Tzetlin, 1991). Obviously the progenedc evolution has been very successful and has triggered an

adaptive radiation.

The egg diameter varies between 240-320 pm in 0. cosmetandra (Oug, 1990) and 56.5 pm in 0. paralabidon

(Hilbig & Blake, 1991). At the end of the brooding period, the progeny of some species is released as

polytrochous larvae with no setigerous segments, whereas other species release juveniles with up to 5 setigers. In

O. vivipara die progeny has only 2-3 setigers when released, but die largest recorded viviparous progeny of O.

socialis had 1 2 setigers.

In summary, die variability in reproductive traits in die genus Ophryotrocha makes ii an extremely valuable

study material, a kind of marine Drosophila. "This genus may be very important for sex allocation studies, since it

contains all three of the basic forms of sexuality found in animals" (Charnov, 1 982, p 20 1 ).

REFERENCES

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AKESSON, B.. 1972b. — Sex determination in Ophryotrocha labronica (Polychaeta. Dorvilleida). In: B. Battaglia (ed). Fifth

European Marine Biology Symposium. Piccin Editore, Padova : 163-172.

AKESSON. B.,1973. — Reproduction and larval morphology of five Ophryotrocha species (Polychaeta. Dorvilleidae). Zool.

Scr., 2 : 145-155.

AKESSON. B..1976. Morphology and life cycle of Ophryotrocha diadema. a new polychaete species from California.

Ophelia. 15 : 23-35.

Akesson. B.. 1977a. — Parasite-host relationships and phylogenetic systematics. The taxonomic position of Dinophilids.

Mikrofauna Meeresboden. 61 : 19-28.

Akesson. B., 1977b. — Crossbreeding and geographic races: Experiments with the polychaete genus Ophryotrocha.

Mikrofauna Meeresboden. 61 : 11-18.

AKESSON. B..1978. A new Ophryotrocha species of the labronica group (Polychaeta. Dorvilleidae) revealed in cross¬

breeding experiments. In: B. BATTAGLIA & J.A. BEARDMORE (eds). Marine Organisms. Genetics. Ecology and Evolution.

Plenum Press. New York and London : 573-590.

Akesson, B.. 1982. — A life table study on three genetic strains of Ophryotrocha diadema (Polychaeta. Dorvilleidae).

/menial. J. Invertebr. Reprod.. 5 : 59-69.

Akesson. B..1984. Spcciation in the genus Ophryotrocha (Polychaeta. Dorvilleidae). In: A. Fisher & H.-D. PFANNENSTIEL

(eds). Polychaete Reproduction. Progress in Comparative Reproductive Biology. Fortschc Zool.. 29 : 299-316.

Bacci, G.. 1978. — Genetics of sex determination in Ophryotrocha (Annelida, Polychaeta). In: B. Battaglia & J.A.

BEARDMORE (eds). Marine Organisms. Genetics. Ecology and Evolution. Plenum Press. New York and London : 549-571.

Bacci. G.. Lanfranco, M.. MANTELLO. I. & TOMBA, M., 1979. A new pattern of hermaphroditism (inducible

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B. AKESSON

Danse, K., 1963. — Polychaetous Annelids from Puget Sound and the San Juan Archipelago. Washington. Proc. biol, Soc.

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BERGLUND. A.. 1991. — To change or not to change sex: a comparison between two Ophryotrocha species (Polychaeta). Evol

Ecol., 5:128-135.

Blake. J. A. .1985. — Polychaeta from the vicinity of deep-sea geothermal vents in the Eastern Pacific. I. Euphrosinidae.

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101.

CHARNOV. E.L., 1982. — The theory of sex allocation. Princeton Univ. Press. Princeton, New Jersey, 355 pp.

CLUTTON-BROCK. T.H., 1991. — The Evolution of Parental Care. Princeton Univ. Press, Princeton, New Jersey, 352 pp.

Hartmann. M., 1943. Die Sexualitdt. Gustav Fischer, Jena, 393 pp.

HERMANS, C.O., 1969. — The systematic position of the Archiannclida. Syst. Zool.. 18 : 85-102.

HlLLBIG, B. & BLAKE, J.A., 1991. — Dorvilleidae (Annelida: Polychaeta) from the U.S. Atlantic slope and rise. Description of

two new genera and 14 new species, with a generic revision of Ophryotrocha. Zool. Scr., 29 : 147-183.

Hogarth, P.J.. 1976. — Viviparity. Edvard Arnold, London, 69 pp.

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Martin. D.. Abello, P. & Cartes, j.. 1991. — A new species of Ophryotrocha (Polychaeta: Dorvilleidae) commensal in

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OCKELMANN, K.W. & Akesson. B.. 1989. Ophryotrocha socialis n.sp., a link between two groups of simultaneous

hermaphrodites within the genus (Polychaeta, Dorvilleidae). Ophelia. 31 : 145-162.

OUG. E., 1990. Morphology, reproduction, and development of a new species of Ophryotrocha (Polychaeta, Dorvilleidae)

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Richards. T.L.. 1967. — Reproduction and development of the polychaete Stauronereis rudolphi , including a summary of

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ROLANDO, A.. 1982. Sexual conditions in a population of Ophryotrocha robusta (Annelida. Polychaeta) from Genoa.

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SCHROEDER, P.C. & Hermans, C.O.. 1975. Annelida; Polychaeta. In: A.C. GlESE & J.S. PEARSE (eds), Reproduction of

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Shine, R.. 1978. — Propagule size and parental care. The "safe harbor" hypothesis. J. thcoret. Biol., 75 : 417-424.

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417-466.

SwEDMARK, B.. 1964. — The interstitial fauna of marine sand. Biol. Rev., 39 : 1-42.

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35

WESTHElDE, W.. 1984. The concept of reproduction in polychaetes with small body size: adaptations in interstitial species.

In\ A. FISCHER & H.-D. PFANNENSTIEL (eds), Polychaete Reproduction. Progress in Comparative Reproductive Biology.

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WESTIIEIDE. W.. 1985. The systematic position of the Dinophilidae and the archiannclid problem. In: S. CONWAY Morris

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ZUNARELLI-VANDINI. R.. 1967. — Azioni reciproche sullc gonadi in coppie omeospecifiche ed eterospecifiche di

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Source : MNHN. Paris

2

Environmental influences on endocrine systems

controlling reproduction in Polychaetes

Matthew G. BENTLEY , Jem BOYLE * & Allan A. PACEY **

Gatty Marine Laboratory, School of Biological and Medical Sciences

University of Si Andrews, St Andrews KYI 6 8LB. Scotland, U.K.

^present address: Clyde River Purification Board, East Kilbride

Glasgow G75 OLA, Scotland, U.K.

**presenl address: Observaloire Oceanologique, LIRA CNRS 671

B.P.28. 06230 Villefranche-sur-Mer, France

ABSTRACT

Photoperiod and/or temperature are known to influence gametogenesis and spawning in a number of polychaete species.

Information is now available on the nature of endocrine systems controlling gametogenesis and spawning in representatives of

several polychaete families. For relatively few species, however, is information available on the possible transduction of

environmental signals by the endocrine system (BENTLEY & PACEY, 1992). We report here on the effects of photoperiod and

temperature on the action of gonadotropin and spawning hormones in the polychaete Nephtys hombergii, and on the action of a

gonadotropin hormone in the polynoid Hannolhoe imbricata.

RESUME

Influences dcs factcurs externes sur les systemes endocrines controlant la reproduction chez les Polychetes

La photoperiode ct/ou la temperature agissent sur les processus de gametogenesc et de ponte chez un grand noinbre

d’especes de polychetes. Si les differents types de systemes endocrines qui controlcnt la gametogenese et la ponte sont bien

documents chez de nombreuses especes de polychetes. on a, par contre, ties peu d* informations sur les interactions existant

entre les facteurs du milieu et ces systemes endocrines (Bentley & PACEY, 1992). Nous rapportons ici les effets de la

photoperiode et la temperature sur Faction de Fhormone gonadotropique et de F hormone de ponte chez Nephtys hombergii

ainsi que sur Faction de Fhormone gonadotropique, qui a recemment ete decrite, chez Harrnothoe imbricata.

INTRODUCTION

Nephtys hombergii Savigny, 1818 (Nephtyidae) mid Harrnothoe imbricata L., 1769 (Polynoidae) arc both

iteroparous polychaetes witii an annual cycle of reproduction. Nephtys hombergii produces a single batch of

gametes which are spawned in late April or May in populations around the coast of northern England or Scotland

(Olive, 1978; Bentley et ai , 1984). Harrnothoe imbricata , in contrast, produces two consecutive batches of

gametes which are produced and spawned in quick succession in the spring (Daly, 1972, 1974; Garwood,

BENTLEY. M.G.. BOYLE, J. & A. A. PACEY, 1994. — Environmental influences on endocrine systems controlling

reproduction in Polychaetes. In: J.-C. Dauvin, L. Laitbif.r & D.J. REISH (Eds). Actes de la 4eme Conference internationale

des Polychetes. Mem. Mus. natn. Hist . not., 162 : 37-44. Paris ISBN 2-85653-214-4.

Source : MNHN. Paris

38

M.G. BEN TLEY. J. BOYLE & A. A. PACEY

1981). Gametogcnesis and spawning in N. hombergii arc controlled by two hormones, a gonadotropin hormone

and a spawning hormone (Olive, 1976: Olive & Bentley, 1980; Bentley & Olive, 1982; Olive & Lawrence,

1990) but to dale, evidence for the influence of any environmental factors on reproduction has been speculative. A

possible correlation was reported, for example, between insolation and daytime spawning of Nephtys caeca

(Bentley et a I ., 1984).

.Studies on Harmoihoe imbricata have revealed a sophisticated photoperiodic control of reproduction

(Garwood & Olive, 1978, 1982; Clark, 1988) but, only recently has a gonadotropin hormone been shown to

operate in the control of oogenesis (Olive et ai, 1990). The first cohort of oocytes requires appropriate

environmental input and endocrine support. The second oocyte cohort has been shown to develop autonomously,

apparently without environmental control.

The results we describe in this paper show that in Nephtys hombergii environmental conditions under which

animals are maintained may affect resorption and the onset of renewed gametogcnesis. Resorption has been shown

to be a common occurrence following spawning failure in this species (Olive et ai , 1981). We also show that

there is endocrine support of development of the second cohort of oocytes in Harmothoe imbricata even though

these do not require continued environmental support. In light of the fact that rapid growth of the first cohort of

oocytes occurs under gonadotropin support apparently associated with increasing photoperiod in the spring

(Clark, 1988) then observations that continued gonadotropin secretion occurs, without further environmental

stimulus, during the rapid vitellogenesis of the second oocyte cohort are as would be predicted.

MATERIALS AND METHODS

Collection and maintenance of specimens. — Specimens o (Nephtys hombergii were collected by digging in

sand at low water of spring tides from three sites: The Black Middens' in the estuary of the River Tyne, North-

East England; Kirkcolm, Wigtownshire, Scotland and from Fairlie Sands, Ayrshire, Scotland. Individuals were

maintained in the laboratory in groups of four in polyethylene containers containing 200ml sea water and sterilised

sand to a depth of 1cm.

Specimens of Harmoihoe imbricata were collected from beneath stones from the intertidal rocky shore at St.

Andrews and Kingsbams, Fife, Scotland. They were maintained individually in small glass jars containing 50ml

of seawater. An empty Patella vulgata shell was included to provide shelter. Animals which were not used within

one week of collection were fed weekly with pieces of Nereis diversicolor presented in forceps.

Light temperature regimes for laboratory maintenance of animals. — Animals were maintained in the

laboratory in Gallenkamp cooled incubators with timed light cycling under a variety of environmental conditions

as appropriate. The particular combinations of photoperiod and temperature were as follows:

Ambient conditions

Summer conditions of daylcngth and temperature 16L: 8D, 15°C

Winter conditions of daylcngth and temperature 8L: 16D, 5°C

Winter daylength/ summer temperature 8L: 16D, 15°C

Continuous illumination, 7°C.

Sampling of coelomic / ovarian oocytes. — Nephtys hombergii were anaesthetized in 0.07% 3-aminobenzoic

acid ethyl ester (Sigma Chemical Co.) in sea water. Samples of coelomic / ovarian oocytes were obtained by

puncturing the body wall in the inter-parapodia! region with a pulled micro-pipette which had been moistened

with filtered sea water. Examination was carried out on a Leitz Diaplan compound microscope using a x40

objective lens.

Extraction of brain homogenates and their preparation for use in tissue culture. — Supra-oesophageal ganglia

(“brains”) were removed from Nephtys hombergii anaesthetized as described above by making a transverse

incision in the dorsal body wall just posterior to the prostomium. Excised ganglia were kept on ice until

homogenization. Homogenization was carried out using an MSE Soniprep 150 ultrasonic disintegrator fitted with

a 9mm titanium steel probe. Crude extracts to be used for immediate bioassay or to be lyophilised for storage were

homogenised in bidistilled water, die aqueous supernatant was then used for injection or lyophilised and stored at

-20°C until used. Heat treated homogenate was prepared by suspending tubes containing crude homogenate in a

water bath at 100°C for I min followed by centrifugation in an MSE micro-centaur; the supernatant was then used

for subsequent addition to tissue culture wells.

Bioassay procedures for SI I in Nephtys. — The bioassay of extracts of supra-oesophageal ganglia for

Spawning Hormone (SH) activity was carried out as follows: gravid specimens of Nephtys hombergii were

Source :

ENVIRONMENTAL-ENDOCRINE INTERACTIONS IN POLYCHAETES

39

anaesthetized as above and injected with extract to be assayed or with filtered sea water as a control. Injections of

lOjil volume were made with a pulled, calibrated glass micropipette. The animals were then placed in an incubator

at 12°C and allowed to recover from the anaesthetic. The spawning response was measured using standard counts

of spawned gametes as described previously (Olive & Bentley, 1980).

Aseptic techniques. — Culture method. Animals were placed in streptomycin (2.5 mg/ml) and penicillin

(5000IU/ml) for a period of 24 h before dissection of ovaries for tissue culture. Animals were anaesthetized as

described above and ovaries were removed by excision of parapodia and lifting out of the ovaries with sterile

watchmaker's forceps. The ovaries from several females were pooled for use in amino-acid incorporation

experiments, where they were explained into culture wells of Cel-Cull 24-well plastic tissue culture plates

(Sterilin) each containing 2 ml of culture medium developed by BENTLEY & Olive (1982) for polychaete organ

culture.

Radio-isotope procedures. — Ten ovaries were added to each tissue culture well. L-[4,5-I I3] leucine

(Amersham International; specific activity 130-190 Ci.mM"1) (=*10,000 counts, well'1) ). The plates were placed in

sealed containers with moist tissue and kept in Gallenkamp cooled incubators at 15°C.

Harvesting of Cultures. — After culture periods of 96 h the ovaries and medium were removed from the wells

and centrifuged briefly in an MSE micro-centaur to sediment the ovaries. The medium was discarded, the ovaries

were resuspended in 1ml of 0.125 M Tris-HCl buffer at pH 8.5 and then homogenised in a Potter glass

homogeniser. An aliquot of 0.5 ml (50%) of the homogenate was stored for subsequent protein analysis using the

Bradford micro-protein determination method (Bradford, 1976). Three ml of ice-cold TCA was added to the

remaining 0.5 ml of homogenate mid this was left overnight at 4°C. The samples were centrifuged (at 2800g) in a

MSE Mistral 3000 centrifuge for 30 min at 4°C. The supernatant was removed and 1ml of 0.15M NaOH was

added to redissolve the proteins. The sample was divided into two, 3 ml Packard emulsifier scintillant 299 was

added mid the sample was then counted for 10 min on a Packard 2000 Tri-Carb liquid scintillation analyzer.

RESULTS

Observations on Nephtys gametogenesis. — Means and ranges of oocyte sizes in individuals which had been

maintained under conditions of: a) winter photoperiod (8L: 16D) and temperature (5°C); c) summer pliotoperiod

(16L:8D) and temperature (15°C); d) continuous illumination at 7°C; or b) recently collected from the field in

September 1990 are represented in Fig. 1. It can be seen that group a) which had been maintained under winter

conditions six of the 19 individuals had no vitellogenic eggs (diameter > 50 |im ) and the mean oocyte diameter

was <80 |im in eight of them. In contrast large vitellogenic eggs were found in virtually all worms in the other

three groups. These observations were made on individuals taken from a field population which did not spawn in

1990 and which at the commencement of the experiment had unspawned vitellogenic oocytes in the coelom. It is

quite clear that resorption of unspawned oocytes is accelerated in individuals maintained under conditions of

winter temperature and photoperiod. Maintenance under low temperature alone (d) does not have the same effect.

Observations on Nephtys spawning hormone activity. — The results of assay of spawning-inducing activity of

Nephtys hombergii supra-oesophageal ganglia taken from individuals which had been maintained under a range of

photoperiod/ temperature regimes for a period of 219 days (from prior to the winter solstice) are shown in Fig. 2.

Individuals injected with supra-oesophageal ganglion homogenate prepared from freshly collected animals show a

response typical of Nephtys hombergii , both in terms of the numbers of gametes released and the percentage of

individuals responding. The response is seen to be highly variable between individuals in that some individuals

spawn out almost completely whereas others spawn only partially. Groups injected with supra-oesophageal

ganglion homogenate prepared from individuals maintained under ambient conditions or under conditions of

winter photoperiod and temperature showed a response similar to that in individuals described above. Groups

injected with supra-oesophageal ganglion homogenate prepared from individuals maintained under summer

conditions, or under conditions of winter photoperiod and summer temperature showed a very low level of

response or no spawning at all.

Observations on gonadotropin hormone activity in Harmothoe imbricata. — Fig. 3 shows the results of amino

acid incorporation into ovaries of Harmothoe imbricata following organ culture for 96 h in the absence or

presence of brain homogenate. Incubation of ovaries of Harmothoe imbricata during the development of the first

cohort of oocytes (8 March 1991) in die presence of brain homogenate and heat treated brain homogenate, and in

medium (all containing H3 leucine) shows enhanced uptake of die amino acid (ANOVA F2,n = 13.04, p=0.001).

40

MG. BENTLEY, J. BOYLE & A. A. PACEY

There is no difference observed on die degree of incorporation between ovaries cultured with fresh or heat-treated

brain homogenate.

a: 8L:16D 5oC, September 1990

20-1

10 -

-o

- 1 - 1 - r - 1 - 1 - 1

0 40 80 120 160 200 240

Oocyte diameter pm (mean and range)

20

■5 10-

ci 16L:8D 15oC, September 1990

40 80 120 160 200 240

Oocyte diameter pm (mean and range)

20

io-

b: Field population September 1990

40

i —

120

160 200

— i

240

Oocyte diameter pm (mean and range)

20

« 10

?2

>

'•5

a

o

d: Constant illumination 7oC

September 1990

40 80 120 160 200 240

Oocyte diameter pm (mean and range)

FIG. 1. — Oocyte diameters (means and ranges) in individuals of Nephtys hdmbergii which have been maintaind for a period

of six months in the laboratory, and from the field in September 1990. The treatment groups were: a) maintained under a

8L:16D photoperiodic regime at 5°C, b) field collected animals, c) maintained under a 16L: 8D photoperiodic regime at

15°C. d) maintained under constant illumination at 7°C. It should be noted that, following spawning failure in the spring,

individuals collected from the field in September still posess vitellogenic oocytes in the coelom.

Incubation of ovaries during the development of the second cohort of oocytes (29 April 1991) in the presence

of brain homogenate prepared either from supra-ocsophageal ganglia excised during development of die first or

second oocyte cohorts also show enhanced uptake of die amino acid compared to the controls (ANOVA F2,i7 =

4.07, p=0.039) but there is no significant difference between die two brain homogenate treatments. This

demonstrates quite clearly the effect of gonadotropin hormGne on ovaries during die development of both the first

and second oocyte cohorts.

DISCUSSION

1 he reproductive cycle ol Nephtys hombergii is known to be controlled by two reproductive hormones (a

gonadotropin and a spawning hormone) which are supposed to be secreted in a cyclical manner during the annual

reproductive cycle (Olive, 1976, Olive & Bentley, 1980; Olive et cii, 1985). It has also been reported that

Source :

ENVIRONMENTAL-ENDOCRINE IN TERACTIONS IN POLYCHAETES

41

Nephtys hombergii is seen to undergo periodic spawning failure which may have an adaptive significance (Olive

et al., 1981). These spawning failures may occur in one of two ways: die production of a cohort of normal oocytes

which are not released as a result of failure to secrete spawning hormone, or (he premature resorption of gametes

prior to the breeding season. It has been proposed that spawning failure and oocyte resorption may occur in

response to ‘poor condition' of the individual (measured by energy levels in die soma) (Olive et al., 1985). The

endocrine system is the means by which environmental (and somatic energy level) information is likely to be

transduced. The results reported here on Neplitys hombergii suggest dial photoperiod may influence die rate of

oocyte resorption in unspawned oocytes and die onset of renewed gametogenesis. Short photoperiod appears to

accelerate this process. Temperature does not appear to exert a marked effect. Photoperiod provides an accurate

means of determining die timing of reproduction (BENTLEY & Pacey, 1992) whereas temperature cycles are less

predictable and are variable from year to year.

id

Z

z

£

<

a.

oo

TREATMENT

FIG. 2. — Spawning response in Nephtys hombergii injected with supra-oesophageal ganglion homogenate which had been

obtained from individuals which had been maintained in the laboratory for a period of 219 days (from prior to the winter

solstice) under: a) ambient photoperiod and temperature, b) a 8L:16D photoperiodic regime at 5°C, c) a 16L: 8D

photoperiodic regime at 15°C, d) a 8L:16D photoperiodic regime al 15°C, or which had been obtained from individuals

recently collected from the field. Control injected animals recieved a dose of lOpl of filtered seawater (solvent vehicle).

Standard counts were those as used by Olive and Bentley ( 1980).

Observations on the production of spawning hormone in Nephtys hombergii show a rather different pattern.

Prolonged exposure to short photoperiod alone is not sufficient to induce production of the hormone in the

supraoesophageal ganglion. Low temperature, in contrast appears to induce spawning hormone production.

Clearly production of spawning hormone is not critical in the timing of reproduction (only the tuning of release

plays a role in this respect), and temperature, therefore, may be an appropriate way of ensuring SH production.

Observations on the field spawning of Nephtys caeca (BENTLEY et al ., 1984), and Nephtys hombergii may be

similar, suggest that temperature may act as a ‘trigger' for spawning. Temperature has been shown to play a role in

controlling spawning of Nereidae (Goerke, 1984) in which there are temperature "windows" for the swarming of

species which are related to their geographical range. It is clear that die control of gametogenesis, hormone

production and readiness to spawn in N. hombergii is a complex process in which temperature and photoperiod

both appear to be involved.

There are few polychaete species in which both environmental and endocrine control of reproduction have

been demonstrated. FRANKE (1983) has demonstrated the transduction of environmental information by the

endocrine system of Typosyttis prolifera in an elegant series of experiments, but there arc at present no other well

42

M.G. BENTLEY. J. BOYLE & A. A. PACEY

documented cases. The reproductive cycle of Harmothoe imbricatci is controlled in a sophisticated manner by

environmental factors, of which photoperiod is the most important (Garwood & Olive, 1978, 1982; Garwood ,

a: March 8, 1991

***

***

□ Control

□ Brain Homogenate

□ Heat treated Brain homogenate

Treatment

FIG. 3. — Incubation of ovaries of Harmothoe imbricatci during: a) the development of the first cohort of oocytes (8 March

1991) in the presence of brain homogenate and heat treated brain homogenate, and in medium (all containing L-[4,5-H3]

leucine) and b) the development of the second cohort of oocytes (29 April 1991) in the presence of brain homogenate,

prepared either from supra-oesophageal ganglia excised during development of the first or second oocyte cohorts, and in

medium only.

1980; Clark, 1988). Photoperiod acts to promote gametogenesis and to prevent abortion of the developing first

cohort of oocytes (Clark, 1988), and this information is relayed to the developing oocytes, at least in part, by a

gonadotropin hormone (Olive et a! ., 1990). The second cohort of oocytes, which develops independently of

continued environmental input, we have demonstrated to be still under the gonadotropin hormone support. It may

Source :

ENVIRONMENTAL-ENDOCRINE INTERACTIONS IN POLYCHAETES

43

be Lliat once gonadotropin hormone secretion is switched on and the critical exposure to short days has been

passed, secretion of die gonadotropin hormone cotinues throughout the development of the two oocyte cohorts.

ACKNOWLEDGEMENTS

The authors are grateful to Dr. Marianne Ghyoot for checking the French abstract. This work was supported by

a Natural Environment Research Council grant (GR3/6841) to MGB.

REFERENCES

Bentley, M.G. & Pachy, A. A.. 1992. Physiological and environmental control of reproduction in polychaetes. Oceanogr.

Mar. Biol. Ann Rev., 30 : 443-481.

BENTLEY, M.G. & Olive, P.J.W., 1982. — An in vitro assay for gonadotrophic hormone in the Polychaetc Nephtys hombergii

Sav. (Nephtyidac). Gen. Comp. Endocrinol.. 47 : 467-474.

BENTLEY, M.G.. Olive, P.J.W., Garwood. P.R. & Wright, N.H., 1984. — The spawning and spawning mechanism of

Nephtys caeca (Fabricius. 1780) and Nephtys hombergi Savigny. 1818 (Annelida: Polychaeta). Sarsia , 69 : 63-68.

BRADFORD, M.M.. 1976. — A rapid and sensitive method for the quantification of microgram quantities of proteins using the

principle of protein dye binding. Anal. Biochem.. 72 : 248-254.

Clark. S., 1988. A two phase photoperiodic response controlling the annual gametogenic cycle in Harmothoe imbricata

(L.) (Polychaeta: Polynoidae). Invertebr. Reprod. Dew. 14 : 245-266.

Daly, J.M.. 1972. — The maturation and breeding biology of Harmothoe imbricata (L.) (Polychaeta: Polynoidae). Mar. Biol.

12 : 53-66.

Daly. J.M.. 1974. — Gametogenesis in Harmothoe imbricata (Polychaeta: Polynoidae). Mar. Biol.. 25 : 35-40.

FraNKE, H.-D., 1983. — Endocrine mechanisms mediating light-temperature effects on male reproductive activity in

Typosyllis pro life ra (Polychaeta. Syllidae). Wilhelm Roux1 Arch. Dev. Biol.. 192 : 95-102

Garwood. P.R.. 1980. The role of temperature and daylength in the control of the reproductive cycle of Harmothoe

imbricata (L.) (Polychaeta: Polynoidae). J. Exp. Mar. Biol. Ecol. , 47 : 35-53.

Garwood, P.R.. 1981. — Observations of the developing female germ cell in the polychaete Harmothoe imbricata (L.). Ini. J.

Invertebr. Reprod., 5 : 333-345.

GARWOOD. P.R. & Olive. P.J.W., 1978. — Environmental control of reproduction in the polychaetes Eulalia viridis and

Harmothoe imbricata. In: D.S. McLuSKY & A.J. BERRY (eds). Physiology and Behaviour of Marine Organisms.

Pergamon Press, Oxford. New York : 331-339.

Garwood. P.R. & Olive, P.J.W., 1982. The influence of photoperiod on oocyte growth and its role in the control of the

reproductive cycle of the polychaete Harmothoe imbricata (L.). Int. J. Invertebr. Reprod., 5 : 161-165.

Goerke, H.,1984. — Temperature dependence of swarming in North Sea Ncreidac. In: A. FISCHER & II. -D. PFANNENSTIEL

(eds), Polychaetc Reproduction. Fortschr. Zool., 29 : 39-44.

Olive, P.J.W. 1976. — Evidence for a previously undescribed spawning hormone in Nephtys hombergii (Annelida:

Polychaeta). Gen comp. Endocrinol., 28 : 454-460.

Olive, P.J.W.. 1978. Reproduction and annual gametogenic cycle in Nephtys hombergii and N. caeca (Polychaeta:

Nephtyidae). Mar. Biol.. 46: 83-90.

Olive. P.J.W. & BENTLEY, M.G., 1980. — Hormonal control of oogenesis, ovulation and spawning in the annual reproductive

cycle of the polychaete Nephtys hombergii Sav. (Nephtyidae). Int. J. Invertebr. reprod. Dew, 2 : 205-221.

Olive. P.J.W.. BENTLEY. M.G.. Wright. N.M. & MORGAN. P.J., 1985. — Reproductive energetics, endocrinology and

population dynamics of Nephtys caeca and N. hombergi. Mar. Biol., 88: 235-246.

Olive. P.J.W.. Clark, S. & Lawrence, A., 1990. Global Warming and Seasonal Reproduction: Perception and

Transduction of Environmental Information. In: M. IIOSHI & O. Yamashita (eds). Advances in Invertebrate

Reproduction. Volume 5. Elsevier. Amsterdam, pp. 265-270.

Olive. P.J.W., Garwood. P.R. & Bentley. M.G., 1981. Oosorption and reproductive failure in Polychaeta in relation to

their reproductive strategy. Bull. Soc. Zool. Fr., 106 : 263-268.

OLIVE, P.J.W. & Lawrence, A.. 1990. Gonadotrophic hormone in Nephtyidae (Polychaeta: Annelida): Stimulation of

ovarian protein synthesis. Invertebr. Reprod. Dev., 18: 189-196.

Source : MNHN. Pahs

3

Morphometric analysis of cellular specification

in Platynereis and Pomatoceros embryogenesis

(Annelida, Polychaeta)

Adriaan W.C. DORRESTEIJN & Craig Marc LUETJENS

Zoologisches Institut (Abteilung 1) der Universitat Mainz

SaarstraBe 21, D-55099 Mainz, Germany

ABSTRACT

Despite differences in size and yolk content, the eggs of two sibling species. Platynereis dumerilii and

P. massiliensis , show the same asymmetrical mode of cytoplasmic segregation. The largest part of the yolk-free

cytoplasm is shunted into the D-quadrant alter second cleavage. The specific cleavage behavior of the D-cell-line

suggests a causal relation between cytoplasmic specification, speed of cell cycles and determination. We have expanded

our morphometric analysis to the development of Pomatoceros triqueter, a polychaete with equal cleavage. However, we

show that small though significant size difference between the quadrants may foreshadow the future dorsoventral polarity

of this embryo. The largest quadrant cleaves asynchronously with respect to the other three quadrants. As in Platynereis .

the speed of cell cycles of blastomeres are positively correlated with the volume of cytoplasm.

RESUME

Analyse morphometrique de specification des cellules de Platynereis et Pomatoceros (Anne-

lide Polychete)

Malgre dcs differences de taille et de contenu de vitellus. les oeufs des deux espdees proches. Platynereis dumerilii et

P. massiliensis . montrent le meme mode de diversification cytoplasmique. La majeure partie du cytoplasme clair et sans

vitellus est repartie dans le quadrant D apres le deuxieme clivage. Le comportement specifique de clivage de la lignee

cellulairc D suggere une relation entre la specification cytoplasmique, la vitesse des cycles cellulaires et la determination.

Nous avons elargi 1’ analyse au developpement de Pomatoceros triqueter. polychete a segmentation egale. Pourtant nous

pouvons montrer que des differences minimes bien que significatives de taille entre les quadrants seraient indicatrices de la

future polarite dorsoventrale de cet embryon. Le quadrant le plus large se divise asynchroniquement par rapport aux trois

autres. Comme chez Platynereis. les vitesses des cycles cellulaires sont reliees positivement au volume du cytoplasme.

INTRODUCTION

Embryogenesis in polychactous annelids is reg<uded as a textbook example of determinative development. In

many such eggs, structural animal-vegetal polarity is apparent before fertilization and foreshadows the future

DoRRESTEIJN. A. W.C. & C.M. LUETJENS. 1994. Morphometric analysis of cellular specification in Platynereis and

Pomatoceros embryogenesis (Annelida. Polychaeta). In: J.-C. Dauvin, L. Laubier & D.J. REISH (Eds), Aclcs de la 4eme

Conference internationale des Polychetes. Mem. Mus. natn. Hist. nat.. 162 : 45-50. Paris ISBN 2-85653-214-4.

Source : MNHN. Paris

46

A.W.C. DORRESTHIJN & CM. LUETJENS

antero-posterior axis of die trochophore larva. Even in seemingly apolar eggs this first body-axis is sel up shortly

after fertilization (KLUGE, 1991). Apart from the emergence of polar bodies which mark the animal pole, polarity

is also manifested by ooplasmic segregation leading to a polar distribution of cytoplasmic components.

In nereids, the second body-axis, i.e. the dorsoventral axis, is believed to be set up at first cleavage (Wilson,

1892). In Platyn e re is dumeri lii, the first cleavage produces two daughter blastomeres of unequal size: die small AB

blastomere (27% of the total egg volume) and the larger CD blastomere. Dorresteijn (1990) was able to show

that the cytoplasmic composition of these two cells differs as well. Volumetric analysis revealed that

approximately 80% of die yolk-free cytoplasm, which accumulates at the animal pole prior to first cleavage, is

allocated to the large CD blastomere, despite the fact that diis blastomere includes only 73% of die total egg

volume. Experiments in which we have equalized diese volumetric proportions led to a duplication of dorsoventral

polarity, and of the trunk structures of the young worm (DORRESTEIJN, Bornewasser & FISCHER, 1987). These

data thus support die idea dial the establishment of die dorsoventral axis depends on the differential distribution of

bodi volume and cytoplasmic contents between die first two blastomeres.

In die present paper, we describe die developmental principles encountered in die unequally cleaving embryos

of two sibling species of Platynereis and in the equally cleaving embryo of the scrpulid Pomatoceros triqueter. Our

results indicate dial die creation of cytoplasmic asymmetry among the four embryonic quadrants may set up

dorsoventral polarity even in "equally" cleaving polychaetes. The data also suggest a correlation between

cytoplasmic distribution and cell cycle duration in individual blastomeres.

MATERIALS AND METHODS

Platynereis dumerilii and Platynereis massiliensis were kept in laboratory cultures (Hauenschild & Fischer,

1969) at 18 C. The serpulid, Pomatoceros triqueter , was collected from the seabed round Helgoland. For

Platynereis dumerilii, die mode of fertilization was previously described by Dorresteijn (1990). Ferdlized eggs

from P. massiliensis were collected from brood lubes in culture dishes. To induce spawning in Pomatoceros die

calcareous tubes in which the animals live were opened with sturdy tweezers at the narrow, rear end. Subsequent

agitation of the animal's tentacles made diem crawl backwards by which diey exposed themselves at the artificial

hatch in the tube. Males (with pale abdomen) and females (with red abdomen) were pul into separate bowls of

seawater and started spawning spontaneously. The eggs were washed in seawater several times and were then

fertilized with diluted sperm.

A careful estimate of cell cycle duration of individual blastomeres was achieved by evaluating several video-

time-lapse recordings of die development (at 18 °C) of each of the three polychaetous species.

Procedures to collect morphometric data from serial sections (1 pm) were as described by Schneider, Fischer

& Dorresteijn (1992). For the small Pomatoceros embryos, however, we digitized every second 1 pm section in

serial sections.

RESULTS AND DISCUSSION

An intricate combination of pre-cleavage cytoplasmic segregation and unequal first cleavage during normal

development of Platynereis dumerilii creates daughter-blastomeres which differ both in size and in cytoplasmic

composition. This seems an essential initial step to create and propagate cellular diversity in die nereid embryo. At

second cleavage, die small AB blastomere divides equally and there is no sign of cytoplasmic diversification. The

huge CD blastomere which contains the bulk of yolk-free cytoplasm (see introduction), however, cleaves

unequally and die largest pari of this yolk-free cytoplasm is shunted into die D-quadrant. As a result of this

cleavage strategy, the D-cell obtains 60 % of the yolk-free cytoplasm although it includes only 51% of the total

egg volume. Again, the cleavage introduces inequality in blastomere size and simultaneously regulates the

cytoplasmic composition ot the daughter blastomeres with a disproportional increase of yolk-free cytoplasm in the

largest cell, the D-blastomere. The cleavage pattern of die D-quadrant differs from that of the odier quadrants. Two

descendants of the D-cell-line, the somatoblasts 2d and 4d, are formed at fourdi and sixth cleavage, respectively.

Bodi somatoblasts are exceptionally large cells and contain yolk-free cytoplasm almost exclusively. Dorresteijn

(1990) has shown a positive correlation between die amount of yolk-free cytoplasm tuid die speed of cell cycles for

all blastomeres (Fig. 1 ). As a result of die allocadon of yolk-free cytoplasm, these D-quadrant-derived cells, 2d and

4d, proliferate much more rapidly than comparable cells of odier quadrants. The relatively long initial cell cycle of

Source :

PLATYNERE/S AND POMATOCEROS EM B R Y OGEN E SIS

47

2d compared lo its precursor cell ID and its progeny 2d1 and 2d11, despite the fact that it obtained a large amount

of yolk-free cytoplasm, seems to be exceptional. DORRESTE1JN (1990) proposes that the interval between fourth

and fifth cleavage may be elongated due to cellular interactions which imprint dorsoventral polarity at the 16-cell

stage.

30%

e

15

c

y

t

o

P10

l

•CD

•0

•10

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0

20

40

60 80 100

Cell cycle duration (min)

120

140

Fig. 1. — The amount of yolk-free cytoplasm in blastomeres of successive cleavage stages of Platynereis dunierilii is

positively correlated with the rale of cell division. This diagram shows this correlation for the individual

blastomeres. We have labeled some of the data points to show that CD and D-quadrant-derived cells proliferate more

rapidly than other cells. However, cell cycles last longer after cells (even in the D-quadrant. e.g. 2d2 and 3d) have lost

most of their clear cytoplasm.

Recently, we were able to show experimentally that die cleavage characteristics normal to a D-quadrant can

also be observed in more than one quadrant if such quadrants contain sufficient yolk-free cytoplasm (Dorresteijn

& Eich, 1991).

The eggs of the sibling species, P. mcissiliensis , are structurally polar from the start and extremely yolky.

They have more than 10 times the volume and develop nearly four times slower than the eggs of P. dunierilii.

Should the mode of cytoplasmic diversification found and documented by morphometric data for P. dunierilii be

essential for determination of blastomeres, one would expect the development of this closely related species to

follow essentially die same mode, even though the initial properties of such eggs arc not the same. We have

compared our data (SCHNEIDER, Fischer & DORRESTEIJN, 1992) widi early light microscope observations on the

development of this species (WISTINGHAUSEN. 1891), which was dicn called the "nereidogenic form of Nereis

dunierilii" . Unfortunately, W failed to observe certain cleavages which makes die comparison of his proposed cell

lineage tree widi our cell-lineage results impossible.

Our comparative analysis of early development gave interesting insights into the way blastomeres become

eytoplasmically diverse. The difference in size between the AB and CD blastomeres of P. mcissiliensis is less than

in P. dunierilii. The CD blastomere of P. mcissiliensis measures 65 % of the total egg volume, yet contains

approximately 73 % of die total amount of yolk-free cytoplasm. Thus, cytoplasmic diversification at first cleavage

is a feature common to both species. Unlike the development of P. dunierilii , second cleavage of P. massiliensis

is unequal in both blastomeres. The allocation of die yolk-free cytoplasm to the daughter blastomeres of AB is

48

A.W.C. DORRESTEIJN & C.M. LUETJENS

proportional to tlie volumes of these cells. Although A- and B-blastomeres differ in size, there is no cytoplasmic

diversification between these blastomeres. The cleavage in CD, however, allocates the yolk-free cytoplasm in

proportions deviating from Hie relative volumes of Die daughter cells with die largest amount (54 % of the total)

ending up in the D-blastomere, which represents only 45 % of die total egg volume. Again, the cytoplasmic

diversification of the D-quadranl is accomplished by both sibling species. The cytoplasmic specification or the D-

cell-line is followed by a specific cleavage behavior differing in many respects from the other three quadrants. As

in P. clumerilii , the somatoblasts 2d and 4d are large cells, receive almost exclusively yolk-free cytoplasm and

proliferate more rapidly. Although cell cycles are nearly four times longer in P. massiliensis, a time scale

transformation (Pig. 3 from SCHNEIDER, FISCHER & DORRESTEIJN, 1992) shows that the asymmetries in the

sequence of divisions among both species are similar in all cell lines. In the same paper, the developmental

similarity has been confirmed by reconstructions of embryos and shows dial the asynchronies of blastomcre

proliferation, a result of differing cell cycle durations, can, with a few exceptions, be correlated widi die allotments

of yolk-free cytoplasm to the blastomeres of P. massiliensis as well. The stringency of cytoplasmic allocation in

die two species suggests a causal relation between cytoplasmic specification and determination of die D-quadrani.

We have expanded our morphometric analyses onto die development of the serpulid Pomatoceros iriqueter. The

small (60-70 pm in diameter) egg of this polychaete contains only small amounts of yolk. The essentials of

development were described by von DRASCHE (1884) and revised by Groepler ( 1986). According to these authors,

die first and second cleavage are equal and the quadrants develop in radial symmetry. Thus, although differences in

size and composition of the quadrants allow us to identify die quadrants in nereids, identification of quadrants

seems impossible at early stages of Pomatoceros.

However, our own studies of die development of diis small serpulid, partially reviewed by DORRESTEIJN &

Fischer (1988) showed that die blastomeres do not cleave synchronously. Even die second cleavage is slightly

asynchronous in the first two cells, although the interval is less than a minute. Cleavage asynchrony is maintained

60 %t

50

B

l

a

S 40

t

o

m

m

e

10 -

0 --

0

10

•CD

•AB

•0

«A,B,C

•ID

•••|1a-1d

* w« . I

• lid22- id22 | *1."- Id" J,aj. ^d 2

30 40 50 60 70 80

Cell cycle duration (min)

FIG. 2. — In Pomatoceros iriqueter , blastomeres of successive cleavage stages which were studied up the 32-cell-stage

show a positive correlation between the amount of cytoplasm and the rate of cell division. Since the yolk is

distributed homogeneously within the cytoplasm, the blastomere volumes can be used as a measure of the amount of

yolk-free cytoplasm.

Source : MNHN. Paris

PLATYNEREIS AND POMATOCEROS EMBRYOGENESIS

49

and becomes more pronounced at later stages, especially among the macromeres and the different quartets of cells

along the animal-vegetal axis. Morphometry of sectioned and reconstructed embryos shows small, yet statistically

significant size differences between the blastomeres as early as at the two cell stage. The largest cell, which we

shall call CD (according to the rules for the majority of unequally cleaving spiralians), is larger than AB by 3.5%

(SD=1.3%; n=9) of the total egg volume. At the four cell stage, one of the daughter cells of CD is larger than the

other daughter cell by little more than 2%, and larger than the daughter cells of AB by 3% (SD=1.9%; n=9). The

size differences are maintained in the vegetal macromeres, but eliminated in the quartets of micromeres which are

formed towards the animal pole during the third and subsequent cleavages.

Light microscope investigations of living embryos and morphometric analysis of serially sectioned embryos

resulted in a clear and positive correlation between the sizes of individual blastomeres and the rate of cell division.

From the diagram Fig. 2 it becomes clear that once the blastomeres grow smaller cell cycle duration increases. The

first quartet of micromeres (la- Id) divides nearly equally and the daughter cells, la’-ld1, have cell cycles which tire

nearly 20 min longer than those of the mother cell. Since the yolk remains distributed homogeneously throughout

the cytoplasm of the blastomeres, blastomcrc size must be proportional to the content of yolk-free cytoplasm in

the blastomeres, and we can postulate the same correlation between the amount of yolk-free cytoplasm and the rate

of cell division that we had previously found for P. dumerilii. This supports the idea that the small though

significant size differences between the cells of the Pomaioceros 4-cell stage may cause the asynchronous

development of its quadrants, which is reinforced in the macromeres at later stages. This asynchrony in the

development of otherwise equivalent blastomeres introduces a polarity axis perpendicular to the preexisting animal-

vegetal polarity which may well coincide with a dorsovenual axis which, however, has not yet been rigorously

demonstrated in Pomatoceros embryos. For this reason we are studying the development of Pomaioceros beyond

the stages we have investigated so far and focussing on the development of mesodermal stem cells which is a

developmental aspect limited to the D-quadrant only. Should both mesoderm development and precocious cleavage

in one of the quadrants be correlated aspects of development, setting up of cleavage asynchronies might prove an

important factor to acquire blastomeres with different developmental fate.

ACKNOWLEDGEMENTS

The careful maintenance of the animal stocks by Mr.A. Heinen is gratefully acknowledged. The supply of the

animals was made possible by the Laboratoire Arago (Banyuls-sur-Mer, France) and the Biologische Anstalt

Helgoland (Helgoland, Germany). The collection of data for this paper would have been impossible without the

financial support from the Deutsche Forschungsgemeinschaft, Bonn (grant Do 339/1-2).

REFERENCES

DORRESTEIJN, A.W.C.. 1990. Quantitative analysis of cellular differentiation during early embryogenesis of

Platynereis dumerilii. Wilhelm Roux1 Arch. Dev. Biol., 199 : 14-30.

DORRESTEIJN, A.W.C.. Bornewasser, H. & FISCHER, A., 1987. A correlative study of experimentally changed first

cleavage and Janus development in the trunk of Platynereis dumerilii (Annelida, Polychaeta). Wilhelm Roux ' Arch.

Dev. Biol., 196 : 51-58.

DORRESTEIJN, A.W.C. & ElCH. P.. 1991. — Experimental change of cytoplasmic composition can convert determination

of blastomeres in Platynereis dumerilii (Annelida, Polychaeta). Wilhelm Roux' Arch. Dev. Biol., 200 : 342-351.

DORRESTEIJN, A.W.C., FISCHER, A.. 1988. The process of early development. In: W. Westheidk & CO. HERMANS (eds),

T he Ullrastruciure of Polychaetes. Microfauna Marina , Gustav Fischer, Stuttgart, 4 : 335-352.

DRASCHE, R. von. 1884. Entwicklung von Pomatoceros triqueter L. Beit rage zur Entwicklung der Polychaeten, Heft

1 : 1-10, Wien, published privately.

Groepler, W.. 1986. — Die Entwicklung bei Pomatoceros triqueter L. (Polychaeta. Serpulidae) vom befruchteten Ei bis

zur schwimmenden Blaslula. Zool. Beilr. N. F.. 29 : 157-172.

11 AUENSC1IILD, C. & FISCHER, a., 1969. Platynereis dumerilii. Mikroskopische Anatomie. Fortpflanzung.

Entwicklung. Grofies Zoologisches Praktikum, Heft 10b. Gustav Fischer Verlag. Stuttgart, 1-55.

50

A.W.C. DORRESTEIJN & C.MV LIJETJENS

Kluge, B. 1991 - Cytologische Analyse der friihesien Entu'icklungsvorgange bei Platynereis dumerilii (Annelida,

Polychaeta). Thesis, University of Mainz, 245 pp.

SCHNEIDER. S.. FISCHER, A. & DORRESTEIJN, A.W.C., 1992. — A morphometric comparison of dissimilar early

development in sibling species of Platynereis (Annelida. Polychaeta). Wilhelm Roux’ Arch. Dev. Biol., 201 : 243-

256

Wilson. E.B.. 1892. The cell-lineage of Nereis : A contribution to the cytogeny of the annelid body. J. Morph., 6 :

361-480.

WlSTINGHAUSEN, C. von. 1891. — IJntersuchungen iiber die Entwicklung von Nereis Dumerilii. Ein Beitrag zur

Entwicklungsgeschichte der Polychaeten. Mitt. Zool. Star. Neaped, 10 : 41-74.

Source : MNHN. Paris

4

Observations on reproduction and growth of Sabella

spallanzanii (Polychaeta, Sabellidae)

in the Mediterranean Sea

Adriana GIANGRANDE & Angela PETRAROLl

Diparlimenlo di Biologia

University di Lecce

73100 Lecce. Italy

ABSTRACT

A year of observations on a population of Sabella spallanzanii is reported. In situ measurements of tube length and

correlation of this parameter to other variables such as worm length and biomass gave indications on growth-rate.

Reproduction was followed by monthly samples and examination of gonad maturation. Sex ratio and minimal size at

reproduction were also investigated. In the Mediterranean Sea S. spallanzanii showed a fast growth-rate and reproduced

during February. Oogenesis is of extraovarian type and eggs reach 250 pm. The presence of protandric hermaphroditism

is indicated.

RESUME

Observations sur la reproduction et la croissance de Sabella spallanzanii (Polychaeta,

Sabellidae) en Meditcrranee

Des observations sur la reproduction d'unc population de Sabella spallanzanii ont ctd faites pendant une annee. La

longueur des tubes a ete evaluee par des mesures directes des individus dans leur habitat naturel. Une correlation entre la

longueur de tube, la longueur du ver et la biomassc a pu etre demontree. A partir dc ccs correlations, il est possible d'avoir

une indication sur la croissance du ver. Des 6chantillons ont etc recoltes tous les mois pour suivre la reproduction des

individus. La taille minimale des vers a la reproduction et leur sex-ratio ont <$t 6 calcules. La ponte de S. spallanzanii a

lieu au cours de 1’hiver en Meditcrranee. La taille ovocytaire maximale observde a etc de 250 pm. Neanmoins les premiers

stades de la gametogenese n'ont pas ete observes et des observations complementaires sont necessaires. L'espece

presente un hermaphroditisme proterandrique.

INTRODUCTION

Sabella spallanzanii (Gmelin, 1791) is one of the most "popular" Mediterranean polychaetes. It has been used

as an experimental animal in numerous studies, but almost always under die generic name of Spirographis.

Recently PERKINS and KNIGHT-JONES (1991) synonymized Spirographis spallanzanii Viviani with Sabella

Giangrande, a. & A. PETRAROLL 1994. Observations on reproduction and growth of Sabella spallanzanii

(Polychaeta, Sabellidae) in the Mediterranean Sea. In: J.-C. DAUVIN, L. LaUBIER & D.J. REISH (Eds). Actes de la 4eme

Conference internationale des Polychetes. Mem. Mus. natn. Hist. nat.. 162 : 51-56. Paris ISBN 2-85653-214-4.

Source : MNHN. Paris

52

A. GIANGRANDE & A. PETRAROU

penicillus Linnaeus, but suggested to suppress penicillus and other synonyms to stabilize die name Spallanzani i.

They pointed out that the correct name for the species, penicillus , has frequently been used incorrectly for

Sabella pavonina Savigny typical of northern Europe.

Sabella spallanzanii is common along the Italian coast. It can be found in the open sea from 1 to 30 m depth,

as well as in shallow hard bottom areas of harbours, where it reaches high densities. Probably the open sea and die

harbour forms belong to different ecotypes because their behaviour and resistance under laboratory conditions are

different

Despite its wide distribution, and its frequent use in physiological studies (Ivanov, 1908; Fox. 1938;

KlORTSIS & Moraitou, 1965; PARRINELLO & RiNDONE, 1981), its reproduction and life-cycle are poorly known

(McEuen et al.y 1983).

The role of coelomocytes in the maturation of germinal products in some specimens from Naples, which

surely belonged to Sabella spallanzanii. was studied by Dales (1961). While the electron microscopical

investigation on sperm of the species incorrectly referred as Sabella penicillum by Graebner and Kryvi (1973),

should probably be referred to Sabella pavonina.

The present paper deals with a year of observations on in situ growth mid reproduction of a Mediterranean

harbour population of Sabella spallanzanii.

MATERIALS AND METHODS

The study was conducted at the Mai* Grande of Taranto (Gulf of Taranto, Ionian Sea) along an artificial, vertical

cliff. The individuals o (Sabella spallanzanii were distributed in patches. One group measured 2 m deep and 9 m

wide, and was chosen to follow individual growth. In situ measurements of tube length were done by Scuba divers

for about one year. Tubes were measured within an area of 400 cm2, using a plastic square to delimitate the

surface. The tube length was correlated with other features of the worm.

Biomass was estimated as dry weight by drying individuals at 65°C for 24 h. Various sized specimens were

collected monthly from the dense patch under study and from adjacent zones. Size at maturation and sex ratio were

determined. Coelomic fluid was analyzed in the laboratory to examine for sexual maturation.

Specimens were fixed in 5 % glutaraldehyde buffered to pH 7.4 and post-fixed for one hour in 4 % osmium

tetroxide for histological studies. For light microscopy, 1 pm thick sections were cut with a glass knife. Thin

sections were cut on an ultramicrotome with a diamond knife for electron microscopy

The temperature cycle was typical of Mediterranean confined environments with a range of 1 1 °-29 °C. Salinity

values were stable at approximately 38 P.S.U.

RESULTS

Density, growth and biometry. Individuals of Sabella spallanzanii were located within a suspension

feeder community typical of Mediterranean eutrophic zones such as harbours (TURSI et al ., 1985). At the

beginning of the study in May 1991. only small individuals were present within the patch, and the density was

about 300 ind. nr2. The mean tube length in July 1991 was 10 cm (Fig. la). In April 1992 it was 18 cm, and in

August 1992 it reached 20 cm in length (Fig lb), with a density of about 150 ind. m'2.

The tube length was correlated with the length of the worm (Fig. 2a), biomass (Fig. 2b) and die number of

setigers (Fig. 2c). Biomass was estimated at 60 g. nr2, and 75 g. nr2 in July 1991 and August 1992,

respectively.

The crown of Sabella spallanzanii is asymmetric, with one involute lobe having an arrangement of spiralled

radioles, but spiralization is absent in small individuals (KNIGHT-JONES et al., 1991). Correlation of number of

spirals with length showed dial worms up to 9 cm in lengdi do not show any spiralling, whereas large specimens

from 30 to 40 cm in length have up to 4 secondary spirals (Fig. 2d). The ratio of body lengdi to crown increases

widi increasing body length, from 1.5 to 4.7, as observed for odier species (Giangrande, 1991).

REPRODUCTION

As observed by Dales (1961), germinal products in sexually mature specimens are found in the coelomic

cavity. No germinal products were observed in die coelom from May to July 1991. The content of die coelom was

Source : MNHN. Paris

REPRODUCTION AND GROWTH OF SAB ELIA SPALLANZANII

53

bright orange or brown and had a rich creamy consistency due to the presence of large coelomocytes. These cells

measure up to 70 jam in diameter. The peritoneum appeared hypertrophic in July, 1991. The early stages of

tub# length cm

FlG. 1. — Sabella spallanzanii. a: Frequency histograms of tube length in July, 1991; b: Frequency histograms of tube

length in August. 1992.

germinal products were probably present in August and September, but samples relative to this period were not

obtained. Germinal products were well developed in October, 1991, when eggs measured about 100 pm. They

reached about 200 pm in December, 1991. and males contained spermatids predominantly at an early stage of

maturation. Eggs had completed vitellogenesis and measured 250 pm in January, 1992. (Fig. 3a). and ripe

spermatozoa (Fig. 3b-c) together with late spermatid stages were present in the males. Spawning occurred in

February. Some females still retained a few eggs surrounded by a large number of coelomocytes in March. The

coelom of the worms was once again full of coelomocytes in April, 1992, and no germinal products were present.

As observed by Dales (1961 ) the quantity of coelomocytes decreased as oocytes matured.

54

A. GIANGRANDE & A. PETRAROLI

SEX RATIO

File minimal size at maturation was computed as 15 cm in length. Specimens from 15 to 20 cm long were all

males ; females occurred only in specimens greater than 20 cm long. The sex ratio was of 1 : 1 in individuals

from 25 to 30 cm. However, males represented more than 80% of the reproductive population when all sized worm

weie considered.

total worm length cm total worm length cm

Fig. 2. — Sabello spallanzanii. a: Correlation between tube length and total worm length; b: Correlation between worm

length and biomass (Dry weight); c: Correlation between worm length and number of setigers; d: Correlation between

worm length and number of spirals of the branchial crown.

Individuals from die patch under observation with tubes measuring about 15 cm in length were all males.

During the period of study no females were present within this patch. Females were found among larger

individuals collected from adjacent zones.

DISCUSSION AND CONCLUSION

Sabella spallanzanii is characterized by a rapid growth rate, l ube length doubled in 10 months. In the

laboratory, it has been reared using many different food sources, and it can be hypothesized that it can feed also on

particulate organic matter. Size distribution within the patch suggested that it could be the product of a single

recruitment episode. The biomass computed per square meter was quite large, even thougth mortality seemed to be

very high during the period of observation, since the density decreased from 300 to 150 ind. nr2.

Spiralization of the radioles represents a growth strategy in large-sized sabcllids. In this way they can obtain an

efficient respiratory and feeding surface without elongation of die crown, diminishing the risk from predation.

Correlation of die number of spirals with body length is important taxonomically, since one of die features used

to distinguish Spirographis from Sabella was die presence of spiralization in the crown.

Reproduction in Sabella spallanzanii seems to be synchronized among individuals. According to Dales

(1961), spawning occurs in winter. 1 Iowever, samples relative to diis first year were not adequate to investigate die

entire gametogenic cycle, especially concerning the appearance of die early stages of germinal development. Data

of the present work suggests that gametogenesis begins in summer. During die gametogenesis, coelomocytes were

observed to decrease in number, especially in females. After spawning die number of coelomocytes increases

Source :

REPRODUCTION AND GROWTH OF SABELLA SPALLANZANI!

55

rapidly and by spring fill the coelomic cavity. Dales (1961) reported that coelomic cells are organized as storage

Fig. 3. — Sabella spallanzanii. a: Electron micrograph of a section through cortex of ripe egg. showing numerous yolk

bodies, magnification 91.000; b-c: Electron micrograph through heads of ripe spermatozoa, magnification 52.000.

centres for the maturation of gametes. Coelomocytes are derived from die peritoneum as small actively phagocytic

cells. Large coelomocytes eventually rupture and liberate their inclusions into the coelomic fluid to be Liken up by

Source

56

A. GIANGRANDE & A. PETRAROLI

younger cells or by gametes. The oogenesis therefore is of the extraovarian type and is classified by Eckelbarger

(1983) as "with numerous amoebocytcs".

The mature egg diameter is 250 pm ; therefore a lecithotrophic development can be hypothesized. Even

thougth the egg diameter does not agree with that of other sabellids having a broadcaster reproductive pattern

(McEUEN et al. , 1983). The structure of spermatozoa is of die primitive type, adapted for external fertilization. It

is of the ect-aquasperm type, which is die most common type among polychaetes. However, die sabellid ect-

aquasperm type was classified by Jamieson & Rouse (1989) as nco-aquasperm, hypothesizing in some sabellids a

re -evolution of ect-acquasperm from ent-aquasperm type. The sperm morphology is very similar to diat described

for Sabella penicillum (GRAEBNER & Kryvi, 1973), but diis is probably a different species from Sabella

spallcinzanii.

Due to die problems existing in die taxonomy of Sabella spallanzanii (Perkins & Knjght-Jones, 1991),

some difficulties arise in comparing present data to odier previous works. For example, Sabella penicillus is

reported to be a dioecious species (McEuen, et al., 1983), but current data, i.e. deviation in sex ratio from 1 : 1

and size of females, supports die hypothesis for the presence in Sabella spallanzanii of a protandric

hermaphroditism, Probably die individuals examined by Dales (1961) were of large size and this led the author to

consider the species as gonochoric. Further investigations are needed to confirm this hypodiesis.

REFERENCES

DALES, P.R.. 1961. — The coelomic and peritoneal cell systems of some Sabellid Polychaetes. Q. J. Microscop. Sci.,

102 : 327-346.

Eckelbarger, K.J.. 1983. — Evolutionary radiation in polychaete ovaries and vitellogenic mechanisms: their possible

role in life-history patterns. Can. J. Zool., 61 : 487-504.

Fox, M.H., 1938. — On the blood circulation and metabolism of sabellids. Proc. Royal Soc. (B). 125 : 554-569.

GIANGRANDE. A.. 1991. Behaviour, irrigation and respiration in Eudistylia vancouveri (Polychaeta. Sabellidae). J.

mar. biol. Ass. U.K.. 71 : 27-35.

GRAEBNER. I. & Kryvi. H.. 1973. The spermiogenesis and mature sperm of Sabella penicillum (Polychaeta). An

electron microscopical investigation. Norw. J. Zool., 21 : 211-226.

Ivanov. P., 1908. Regeneration des vorderen, und des hinleren Korperendes bei Spirographis spallanzanii. Viv.

Zeitschrift f wissensch. zoologie., 91 : 510-558.

Jamieson, B.G.M. & ROUSE, W., 1989. — The spermatozoa of the Polychaeta (Annelida): an ultrastructural review. Biol.

Rev.. 64 : 93-157.

KIORTSIS. V. & Moraitou M.. 1965. Factors of regeneration in Spirographis spallanzanii. In: V. KlORTSIS & II.A.L..

Trampush (cds). Regeneration in Animals and related problems. North Holland Publ., Co., Amsterdam : 250-261.

KNIGHT- JONES, P., Knight-JONES, W.. & Ergen, Z., 1991. — Sabelliform polychaetes, mostly from Turkey's Aegean

coast. J. Nat. Hist.. 25 : 837-858.

McEuen. F.S.. Wu, B.L., & CHI A, F.S.. 1983. — Reproduction and development of Sabella media, a sabellid polychaete

with extratubular brooding. Mar. Biol., 76 : 301-309.

PARRINELLO, N. & RlNDONE, D.. 1981. Studies on the natural hemolytic system of the annelid worm Spirographis

spallanzanii (Polychaeta). Dev. Comp. Immun. N.Y. 5 : 33-42.

PERKINS, T.H. & KlNGHT-JONES, P.. 199 1. — Towards a revision of the genera Sabella and Bispira (Sabellidae). Ophelia.

Suppl. 5 : 698.

1URSI. A.. MaTarrese, A., CECERE. E. & RlBECCO, N., 1985. Sviluppo di popolazioni bentoniche su pannelli fouling

nel Mar Grande di Taranto. Atti S./.T.E. , 5 : 585-589.

Source : MNHN. Paris

5

The functional significance of blood plexuses

in the ecology of Ophelia bicornis Savigny

Tegwyn HARRIS

Departmeni of Biological Sciences

The University of Exeter, Hatherly Laboratories

Prince of Wales Road, Exeter, EX4 4PS, U.K.

ABSTRACT

The anatomy of the anterior blood vascular system of Ophelia bicornis is described with especial reference to its plexuses

of inflatable blind capillaries. The functional significance of these plexuses under the influence of systolic blood pressure and

their roles in the provision of an efficient burrowing mechanism through relatively dilatent sand whilst, at the same time,

helping to maintain an efficient transport system for dissolved substances is described and discussed within the context of the

ecology of the polychaete. The study has been carried out by direct observation of the living worm, by dissection and by

analysis of absorbed radioactively-labelled glutamic acid.

r£sum£

Signification fonctionnelle des plexus sanguins pour Pecologie d* Ophelia bicornis Savigny

L'anatomie du systeme vasculaire sanguin anterieur d 'Ophelia bicornis est decrite en considerant plus specialcment ses

plexus de capillaires aveugles et dilatables. La signification fonctionnelle de ces plexus, sous 1’influence de la pression sanguine

lors de la systole, leur role dans la mise en oeuvre d'un mecanisme efficace pour 1'enfouissement dans des sables relativement

compacts el le role qu’ils jouent, dans le meme temps, comme systeme de transfer! des substances dissoutes, sont decrits et

discutes dans le contexte de 1'ecologie du Polychete. L’etude a etc conduite par observation directe d’animaux vivants. par

dissection et par l'analyse d'acide glutamique radioactif absorbe.

INTRODUCTION

The mechanisms of digging into, and travelling through, marine sediments by soft-bodied invertebrates has

been studied at some length. Both in the bivalved molluscs (Ansell & Trueman, 1967: Trueman, 1968) and in

the annelids (Chapman, 1950, 1958), it has been shown that effective locomotion is usually achieved by an

interaction of the body-wall musculature and an internally-developed hydrostatic tension in a body fluid, usually

that which fills the coelom.

The most extensive studies of burrowing in the Polychaeta have involved Arenicola marina. Chapman and

Harris, T., 1994. The functional significance of blood plexuses in the ecology of Ophelia bicornis Savigny. In:

J.-C. DaUVIN, L. LaUBIER et D.J. REISH (Eds), Actes de la 4eme Conference internationale des Polychctes. Mini. Mas. nam.

Hist, not .. 162 : 57-63. Paris ISBN 2-85653-214-4.

Source : MNHN. Paris

58

T. HARRIS

Newell (1947) and TRUEMAN ( 1966a, b) have discussed the nature and mode of action of the hydrostatic system,

whilst WELLS (1944, 1952. 1954. 1961) has described the mechanical activities of the proboscis and their

significance to the behaviour of die worm. The consensus of this work is dial the primary thrusting force is

generated by the interaction of the internal coelomic fluid pressure and die highly-controlled body- wall muscles

and muscular, eversiblc proboscis.

Wells (1954) and Chapman (1958) pointed out that much of die success of this process is due to die presence

in Are ni co la of an open coelom which results in the deployment, at die anterior, of die total force generated by

extensive areas of body-wall musculature reacting against a "whole-body" hydrostatic skeleton. In association

widi diis, WELLS (1954) also suggested that the diree retained anterior septa of Arenicola serve to resist the at-rest

coelomic pressure in order to restrict unnecessary extension of die proboscis. Ophelia bicornis , too. has a coelom

which is continuous throughout die body and two retained anterior septa, but they are used in a manner which is

totally unlike that of Arenicola. This paper reports the mode of acdon of that coelomic apparatus and of the way in

which it is augmented by the acdvities of die complex blood vascular system.

MATERIALS AND METHODS

a. Anatomical and behavioural study.

Ophelia bicornis was collected from Bull Hill Bank in the estuary of die River Exe, Devon, U.K. Worms were

killed and fixed by immersion for about three hours in 5% neutral formalin in sea water, some after fresh-water

narcotisation, others without pre-treatment. This was necessary since, as reported by Brown (1938) for Ophelia

rathkei , die only agent which is effective for die narcotisation of 0. bicornis is fresh water. Immersion in fresh

water for about twenty minutes induces total narcosis and also causes the worm to extend to its full, straight,

length. Since this is clearly induced by osmodc influx of water into die coelomic compartment, all dissections

were performed on narcotised specimens for clarity and repeated on untreated specimens for confirmation of the

exact state of the organs and tissues. In practice, it was found dial even the most delicate coelomic capillaries were

not modified by the fresh-water treatment.

Locomotory activities were observed in Ophelia provided with semi-transparent artificial sand composed of a

mixture of glass beads of appropriate granularity moistened with sea water. Use of immature worms, with

relatively unpigmented and thin body-walls, permitted a certain amount of direct observation of internal activity.

b. Amino acid uptake.

Amino acid uptake was investigated using L-[U-,4C] glutamic acid (50(iCi. cm-3), supplied by Amersham

International, in a laboratory regime based upon "Analar" quality acid-cleaned sand and artificial sea water as

formulated by Dawson et al (1969).

132 pi of radioactive amino acid were added to 75ml of artificial sea water. This was thoroughly mixed and

added to 150 g of sand and cooled to 10 °C. Experiments were carried out at this temperature. Sand prepared in

this way was found to contain sufficient radioactive material to give 39 072 dpm. g'1 sand at die degree of

dampness used in the experiments (dpm = disintegrations, min'1 as counted in the liquid scintillation counter).

Ophelia bicornis were placed in the prepared sand and allowed to burrow naturally.

Individual worms were removed at intervals of 10 min, 20 min. 30min, 45 min and 60 min, rinsed in artificial

sea water and immediately cut into three portions representing die prostomial and pharyngeal region, the mid-gut

(intestinal) region and the hind-gut (chiefly rectal) region. The mass of diesc portions was determined and they

were prepared for liquid scintillation as follows.

The tissue was placed in glass scintillation vials widi 0.9 ml of "Soluene 350" and digested at 40 °C overnight.

After cooling to room temperature, 0.2 ml propan- l-ol and 0.4 ml 30 % hydrogen peroxide in two 0.2 ml portions

over two hours, were added to decolorize die pigmented solution. After the addition of die second portion of

hydrogen peroxide, the samples were heated to 40 °C to drive off excess peroxide and again allowed to cool.

5.0 ml ’’Packard 299" scintillation fluid were added to each vial and die activity of the mixture was measured

in a Packard "Tri-carb 460 CD" liquid scintillation counter by die sample channels mediod against a quench curve

prepared from measurement of vials containing "Packard 299" fluid with chloroform as the quench reagent.

c. Autoradiography.

Worms destined for autoradiographic study were allowed to ingest die radioactive amino acid-treated sand for

two hours prior to fixation. This relatively lengdiy treatment time was decided upon since the aim of the present

BLOOD PLEXUSES AND ECOLOGY OP OPHELIA BICORNIS

59

investigation was solely to determine the extent of amino acid uptake and its broad distribution within the tissues

of Ophelia bicornis.

Worms were fixed in 3 % neutral formalin in sea water without prior narcotisation and. during fixation, were

divided into 1.0 cm long portions so dial the intestine could be cleared of sand. The fixed tissues were dehydrated

through a standard ethanol series, embedded in paraffin wax and sectioned at 10pm. Sections were mounted on

gelatin-subbed slides as recommended by Kodak Ltd (1978) and ROGERS (1979). They were coated with "Kodak’1

AR10 stripping film and allowed to expose, in the dark, at 15 °C for 14 days. The slides were developed in

"Kodak" D-19 and fixed in "Kodak" F-5.

The Ophelia tissues acquired a pale straw colour during processing which rendered them clearly visible

beyond the developed silver, thus obviating the need for staining.

Control of the technique was effected in two ways: a) by comparison with similarly- processed sections of

tissues which had not been subjected to radioactive labelling and, b) by examination of putative developed silver

grains by dark-field microscopy, as recommended by Rogers (1979).

RESULTS

a. The anterior coelom and its vascular system

The overall pattern of the blood vascular system followed the descriptions of Clapar£de (1870) from Ophelia

radiata and of Brown ( 1938) from 0. raihkei. The constructional design is in two major parts, a posterior system

based upon a series of sinuses and an anterior system of complex blood vessels.

The whole length of the intestine of 0. bicornis is surrounded by voluminous dorsal and ventral blood sinuses,

of which the dorsal is the larger. The ventral sinus more nearly resembles an inflated blood vessel and, for most of

its length, is virtually buried within the ventral tissues of the typhlosole.

40mm

FlG. 1. A semi-diagrammatic drawing of the anterior of Ophelia bicornis dissected from the right side and cut back to

beyond the ventral nerve cord. For the sake of clarity the prostomial part of the pharynx is not shown, bw, vessels to the

body-wall. - eg. cephalic ganglion. - cv, commissural vessel. - dv, dorsal blood vessel. - h. heart. - ij, "injector organ". - ijv.

"injector organ" blood vessel. - is, intestinal sinus. - 1, ligaments. - m, position of mouth. - pp. pharyngeal capillary plexus.

- prp. prostomial capillary plexus. - vc, ventral cistcma.

The anterior blood system is illustrated semi-diagrammatically in Fig.l. The conspicuous parts of die system

arise from the junction of the buccal chamber with the intestine (shown at the left of Fig.l). At this point, the

dorsal intestinal sinus gives rise to a muscular heart which contains a non-return flap- valve (Fig.2). From the

heart, an anterior dorsal vessel gives rise to four paired vessels. From posterior to anterior these are - a pair of

lateral vessels which connect the dorsal and ventral sinuses, a pair of vessels which enter the wall of die buccal

chamber, then two pairs of commissural vessels which link widi a sub-pharyngcal cisterna of chambered

Source :

60

T. HARRIS

appearance. The dorsal vessel then passes through the walls of the "injector organ" to the prostomial coelom

where it divides into two anterior lateral vessels which travel back through the "injector organ" wall, apparently

between the two septal components, and continue as afferents to the sub-pharyngeal cistema.

"Blind appendages" or, perhaps more correctly "blind capillaries", arise in large numbers from the anterior

paired vessels, forming a dense plexus surrounding the pharynx and another within the prostomial coelom, as

shown in Fig.l. Cardiac activity produces alternate swelling and deflating of the blind tips of die capillaries: at

cardiac systole, 1.0 - 1.5mm of die tip swells to such an extent Uiat the capillary wall stretches until it is virtually

invisible under die low power of the microscope; at cardiac diastole, the tubular appearance is resumed.

FIG. 2. A median longitudinal section of the heart of Ophelia bicornis, - dv, dorsal blood vessel. - f. the flap valve. - is,

intestinal sinus. The arrows point toward the anterior of the worm.

The increase in volume of the anterior blood system due to die simultaneous inflation of so large a number of

blind capillaries is considerable. It seems that diis activity is of benefit to 0. bicornis in two ways.

The most obvious purpose of die mechanism is perhaps that of putting a large volume of blood, under

pressure, in close contact with the coelomic fluid and its corpuscles. This may be an important means of

producing coelomic fluid by an ultrafiltration process and of transpordng dissolved molecules between the two

body-fluid systems. This view gains some support from die presence of similar blind capillaries on die nephridial

blood vessels of O. bicornis and from the experimental evidence, based upon amino acid uptake, which is

presented below. Studies such as those of KOECHLIN (1966), Nakao (1974) and Ruppert & Smith (1988)

suggest that efficient internal fluid transfer in polychaetes is often effected under pressure across the thin walls of

capillaries, somedmes organised into plexuses. Such efficiency may be achieved in Ophelia bicornis by means of

the inflatable blind capillaries described here.

There is, however, a more spectacular purpose to this system which is of mechanical nature and easily

observed as it occurs widiin die prostomial coelom. The "injector organ", similar to that described by Clapar£de

(1870) in Ophelia radiata, is a structure formed from the two remaining segmental septa, which seals off die

prostomial coelom of Ophelia bicornis from die main body coelom. Observation of acuve 0. bicornis shows diat

the "injector organ" plays an important role in die increasing of prostomial coelomic fluid pressure, but it is a

passive role. 'Hie walls of the organ do not contract to any appreciable extent in 0. bicornis and dierefore little, if

any, of its contained fluid is squeezed into die anterior chamber. The passivity of die "injector organ" and die

relative inelasticity of the prostomial cuticle combine to make the prostomial coelom not only a sealed chamber,

but also a reladvely inexpandable one.

b. The uptake of dissolved amino acids.

Harris (1991b,c) has indicated diat 0. bicornis probably supplements its diet to a very considerable extent by

the uptake of dissolved organic material from die interstitial water and from die surfaces of die sand grains which

are crammed into die gut during the feeding cycle. Investigations using radioactively-labelled glutamic acid have

Source :

BLOOD PLEXUSES AND ECOLOGY OF OPHELIA BICORNIS

61

shown that the radioactive marker accumulates to a greater extent in the anterior part of 0. bicornis than

elsewhere, as shown in Fig. 3. Autoradiographic investigation of thin sections of the anterior region shows that a

considerable proportion of the labelled amino acid accumulates in the coelomic corpuscles of the sealed anterior

chamber. Fig. 4.

Minutes

Uptake of L-(U-uC)gIutamic acid expressed as DPMg1 wet weight Ophelia tissue

FIG. 3. — A bar chart showing typical uptake by Ophelia bicornis of radioactively-labelled glutamic acid over a sixty minute

period. "Anterior" = the prostomium and buccal region, "Mid gut" = the central part of the body containing the absorptive

part of the intestine, "Hind gut" = the rectum and pygidial papillae. DPM = disintegrations per minute in the scintillation

counter.

DISCUSSION

According to Fauvel (1959) "L'appareil circulatoire des S6dentaires prSsente d'innombrables modifications

on rapport avec la specialisation dcs diffdrentes regions du corps." Even within die context of such variety, die

blood vascular system in the genus Ophelia is outstanding bodi in its structural modificadons and in its functional

relationships widi die hydrostatic system and through both, with the behaviour and ecology of die worm.

Clapar6de (1870) described numerous blind vessels on die lateral vessels of Ophelia radiata: "Sur tout ce

parcours le vaisseau dorsal et le vaisseau ventral sont mis en communicadon par une serie d'anses. Le caracterc le

plus rcmarquable de cet appareil e'est que tous ces vaisseaux, surtout le dorsal et les anses, sont munis de

centaines d'appendices aveugles, contractiles, dont le jeu alternatif de systole et de diastole est fort curieux k

observer." He goes on to say that these structures are most numerous in die peripharyngeal region and are

relatively rare within die prostomial coelom.

Clapar£de (1870) described die "injector organ" as being of a tough, muscular nature and important to die

generation of the prostomial rigidity which is so necessary for die penetration of sand. He said that this is

accomplished by die contraction of die "appareil injecteur" by its own musculature, thus forcing into die enclosed

prostomial coelom an additional volume of coelomic fluid, increasing the overall hydrostatic tension against die

cuticle and so inducing a certain stiffness. In O. bicornis die "injector organ" seems to act only as die inclasdc rear

wall of the enclosed prostomial chamber.

At cardiac systole, die prostomial coelomic fluid is put under considerably increased pressure by die sudden

and simultaneous inflation of the blind capillaries of die prostomial plexus. This pressure, developed against the

inelastic cuticle, provides the necessary turgidity for die penetration of sand. At the same time, pressure is brought

to bear on die anterior part of the pharynx which passes dirough die ventral wall of the "injector organ" and

dirough die prostomial coelom and, due to die inflation of die plexus which lies external to the "injector organ",

upon die posterior part of the pharynx also. This greatly facilitates die eversion, through the mouth, of die

62

T. HARRIS

voluminous pharynx (issues. It is probable that this pressure increase is supplemented by an increase in the

volume of the pharyngeal coelomic fluid due to ultrafiltration through the greatly-expanded walls of the blind

capillaries.

Fig. 4. — Autoradiographs of unstained sections of Ophelia bicomis after uptake of radioactive glutamic acid, a: a cross-

section through the anterior pharyngeal region shows scattered concentrations of silver, b: part of the inner wall and

coelom of the "injector organ" shows great concentration of silver in the coelomic corpuscles and scattered grains in the

coelomic fluid. - cc. coelomic corpuscles. - cf. coelomic fluid. - ij. "injector organ". - p, pharynx. - pp. pharyngeal plexus.

Harris (199 lax) described Hie typical habitat of 0. bicomis in the Exe Estuary as being emersed for

considerable periods, well — il not excessively — drained and meagre in potential food-sources and resistant to

passage by a soft-bodied invertebrate. Chapman and Newell (1947). having described die pressure which can be

developed, within die anterior coelom and proboscis of Arenicola marina state, suggested that diis allows the

worm to dig and to burrow effectively only when provided with thixotropic sand. It is not inappropriate to note

therefore, that die hydrostatic mechanism which is described here for Ophelia bicomis allows die worm to travel

at all times with apparent ease dirough sand which is thixotropic for only relatively brief periods and dilatent for

much longer ones.

1 he thinness of the gut-lining wall of the intestinal sinus of O. bicomis probably ensures the rapid transport of

absorbed dissolved substances directly into the blood from the surfaces of die sand grains around which the walls

of the gut wrap themselves in a totally-enveloping manner. This, coupled with the presence of a defaecation-

enhancing device in die rectum (Harris, 1991b), gives an indication of the means which exist for efficient and

constant nutrient uptake in this polychaete. Provision of a swift transport and storage mechanism, making use of

an already-enhanced vascular system, would seem to be a logical ultimate development.

CONCLUSION

The entire cycle of events may be summarised as follows:

a) Ophelia bicomis travels through highly resistant sand. Enhancement of die pressure within its prostomial

hydrostatic skeleton by blood surges into expandable capillaries from a valved heart assists movement through die

substrate.

b) Co-incidentally, the induced pressure system increases die efficiency of pharyngeal eversion and thus the

intake of sand.

c) Nutrients absorbed from dial sand are passed rapidly into the blood stream and efficiently flushed from the

site of absorption to sites of temporary storage.

d) 1 he same vascular apparatus permits rapid interchange of solutes between the blood and die coelomic fluid

and its corpuscles which may act as one of die sites of food storage.

Source :

BLOOD PLEXUSES AND ECOLOGY OF OPHELIA BICORNIS

63

ACKNOWLEDGEMENTS

I am grateful lo Philip Shears for his unfailing and cheerful support in the laboratory and aquarium, to

Margaret Grapes for die benefit of her skill in handling the radio-isotope materials and to my colleague,

Professor David Nichols for his continued interest, advice and constructive criticism.

REFERENCES

ANSELL, A.D. & TRUEMAN, E.R., 1967. — Burrowing in Mercenaria mercenaria (L.) (Bivalvia, Veneridae). J. exp. Biol.. 46 :

105-115.

BROWN, R.S., 1938. The anatomy of the polychaete Ophelia clulhensis McGuire, 1935. Proc. R. Soc. Edinb ., 58 : 135-160

Chapman, G.. 1950. Of the movement of worms. J. exp. Biol.. 27 : 29-39

CHAPMAN, G., 1958. — The hydrostatic skeleton in the invertebrates. Biol. Rev.. 33 : 338-371

CHAPMAN, G. & Newell. G.E.. 1947. The role of the body fluid in relation to movement in soft-bodied invertebrates. I. The

burrowing of Arenicola. Proc. R. Soc., Ser.B, 134 : 431-455

ClaparEde, E., 1870. — Les annelides chetopodcs du golfe de Naples, seconde partie. Mem. Soc. Phys. Hist. nat. Gendve.

20 : 1-225.

Dawson. R.M.C., ELIJOTT, D.C., Elliott, W.H. & JONES, K.M.. 1969. — Data for Biochemical Research. 2nd Edition,

Oxford University Press, 654 p.

FAUVEL, P.. 1959. — Organes des sens. Pages 95-1 19. In P.-P. GrassG (ed), Traiti de Zoologie. 5, Masson, Paris : 95-119.

Harris, T.. 1991a. — The occurrence of Ophelia bicomis (Polychaeta) in and near the estuary of the River Exe, Devon. J.

mar. biol. Ass. U.K.. 71 : 391-402.

Harris, T.. 1991b. - The rectal organ of Ophelia bicomis Savigny (Polychaeta): a device for efficient defaecation. Zool. J.

Linn. Soc., 103 : 197-206.

Harris. T.. 1991c. Some aspects of the specific habitat requirements of Ophelia bicomis (Polychaeta). J. mar. biol. Ass.

U.K. . 71 : 771-786.

Kodak Ltd., 1978. Kodak materials for autoradiography. Kodak Information Sheet P- 64(4): 1-14.

KOECHUN, N.. 1966. — Ultrastructure du plexus sanguin peri-oesophagien; ses relations avec la nephridie de Sabella

pavonina Savigny. C. r. hebd. Seanc. Acad. Sci., Paris. Ser. D. 262 : 1266-1269.

NakaO, T., 1974. — An electron microscope study of the circulatory system in Nereis japonica. J. Morph.. 144 : 217-235

ROGERS. A.W.. 1979. — Practical autoradiography. Amersham International, Amersham.

Ruppert, E.E. & SMrrH, P.R., 1988. — The functional organization of filtration nephridia. Biol. Rev.. 63 : 231-258.

TRUEMAN, E.R., 1966a. — The mechanism of burrowing in the polychaete worm, Arenicola marina (L.). Biol. Bull., 131 :

369-377.

Trueman, E.R.. 1966b. — Observations on the burrowing of Arenicola marina (L.). J. exp. Biol., 44 : 93-1 18.

TRUEMAN, E.R., 1968. — A comparative account of the burrowing process of species of Mactra and of other bivalves. Proc.

malac. Soc. Land.. 38 : 139-150.

Wells, G.P.. 1944. — Mechanism of burrowing in Arenicola marina L. Nature, lx>nd.. 154 : 396.

WELLS, G.P.. 1952. — The proboscis apparatus of Arenicola. J. mar. biol. Ass. U.K., 31:1- 28.

Wells, G.P.. 1954. — The mechanism of proboscis movement in Arenicola. Q. Jl Microsc. Sci.. 95 : 251-270.

Wells, G.P.. 1961. — How lugworms move. Pages 209-233. In: J. A. Ramsay & V.B. WiGGLESWORTH (eds). The Cell and

the Organism. Cambridge University Press : 209-233.

Source : MNHN. Pahs

6

Feed-back regulation in Platy nereis dumerilii

Audouin & Milne-Edwards, 1833:

a status review

Dietrich K. HOFMANN

Department of Zoology & Parasitology

Ruhr-University Bochum

D-4630 Bochum, Germany

ABSTRACT

in Plaly nereis dumerilii , gametogenesis and heteronereid transformations, as well as growth and regeneration of

posterior parapodial segments, proceed under the endocrine control of presumeably a single hormone, which is produced

by and released from the supraoesophageal ganglion. As the universal principle applying to all gonochoric. monotclic

species in the family Nereidae investigated so far, this hormone controls postlarval development in a concentration-

dependent manner. The juvenile growth-phase and the early stages of gametogenesis are determined by high hormone

levels which, simultaneously, prevent precocious maturation and metamorphosis. Decreasing hormone levels correlate

with gamete maturation, heteronereid metamorphosis and. on the other hand, with a loss of regenerative capacity.

Neither oocyte differentiation beyond the critical stage nor spermiohistogenesis require additional hormone. The decline

in hormone concentration in P. dumerilii is not based on a brain-autonomous control of hormone production and release

but results from a more complex system of exogenous and endogenous factors acting on the cerebral ganglia. Severe

amputation of segments in both maturing females and males was, but transection of the nerve cord was not the decisive

factor for brain hormone activation. Removal of oocytes, injection of oocytes or of spermatogenic cells into juvenile

hosts affect hormonal activity, and juvenile prostomia are inactivated when passaged in maturing males. The results arc

interpreted in terms of inactivation (or reactivation respectively) of brain hormone activity, caused by humoral feed-back

emanating from coelomic cells, probably the germ cells. These findings are similar to but not identical with those

concerning brain-body interactions in female Nereis diversicolor and Perinereis cultrifera . Isolation of a low molecular

weight substance has been reported from the latter species, but the retroacting factor(s) in Platynereis dumerilii have not

yet been analysed yet.

RESUME

Revue de la regulation en retroaction chez Platynereis dumerilii Audouin & Milne-Edwards,

1833

Chez Platynereis dumerilii la gametogenese et la metamorphose heteron6r<5idicnne, ainsi que la proliferation ct la

regeneration de segments parapodiaux sont conditionnees par Taction d’une hormone elaboree par les ganglions

c£r6broides. Comme principe universel des especes de Nereidiens h reproduction gonochorique et monotelique, le controlc

Hofmann. D.K.. 1994. -- Feed-back regulation in Platynereis dumerilii Audouin & Milne-Edwards, 1833: a status

review. In: J.-C. DaUVIN. L. LaUBIER & D.J. REISH (Eds). Actes de la 4eme Conference internationale dcs Polycheles.

Mem. Mus. natn. Hist. nat.. 162 : 65-72. Paris ISBN 2-85653-214-4.

Source MNHN. Paris

66

D.K. HOFMANN

hormonal du developpement posllarvairc s'effeclue cn fonction de la concentration de l'hormone. La phase juvenile de

croissancc ct le debut de la gametogenese sont assurees par un taux hormonal elevc, qui, cn meme temps, inhibe la

maturation et l'epitoquie precoce. Le progres de la gametogdnese, de la metamorphose et l'arret de la regeneration

postcricurc sc relient a une diminution progressive de 1'activite endocrine. Par contre l’ovogenese et la spermatogenese,

au dcla d’une phase critique, sont achevees meme sous des conditions anhormonales. La reduction caracteristique du taux de

l'hormone au cours du cycle vital ne resulle pas du conlrolc autonome de la synthese et de la secretion par le cerveau lui-

meme mais ressort d'actions plus complexes de facteurs endogenes et exogenes sur les ganglions cerebroi'des.

L'amputation d'un nombre substantiel de segments posterieurs allure le status endocrine des vers males et femclles

proches de la maturite sexuelle. N6anmoins. la l<5sion de la chainc nerveuse ventrale, due h l’operation, n'est evidemment

pas la cause de la reactivation endocrine cerebrale que Ton constate. Ccpcndant, I'enlevement des ovocytes ou V injection

d'ovocytes submatures (ou de cellules spermatogenetiques) dans le coelome des vers juveniles, influence 1’activite

endocrine du contexte. En plus, des prostomiums prdlevcs sur des animaux juveniles subissent une deactivation du cervcau

au cours d'un passage dans le coelome des males s'approchant dc la maturite. Ces effets sont considcrcs comme le r^sultat

dune retroaction humorale sur I'activitc endocrine cerebrale provenant vraisemblablement des produits genitaux.

L’interdependance humorale entre le corps et le cerveau constat^ chez Platynereis dumerilii est comparable, mais n est pas

tout h fait identique a celle observee chez Nereis diversicolor et Perinereis cultrifera. Une substance provoquant l'arret de

1'activite hormonale cdrebralc a ete isolee des ovocytes de la derniere espece; par contre un factcur analogue n’a pas encore

ete identifie chez P. dumerilii.

INTRODUCTION

Feed-back control means that a controlled system itself is acting back on its own control unit either to

maintain or to alter a given physiological state. In the case of endocrine control of sexual maturation in nereid

polychaetes, a feed-back phenomenon was first described by DURCHON (1952) in Perinereis cultrifera. He

discovered dial oocytes and associated coelomocytes taken from females approaching maturity ("ovocytes

submatures", diameter > 180 pm) and injected into immature males of die same species caused precocious gamete

maturation and epitokous transformation. Since Durchon (1948, 1952) had found out dial maturation mid epitoky

arc controlled by an inhibitory hormone originating from the prostomium, he concluded that die submature

oocytes released a factor which down-regulated this inhibitory hormone, thus enhancing gamete maturation and

heteronereid metamor-phosis. This was the first indication of possible interaction between the endocrine system

and die maturing body.

All available data agree widi die view that, as an universal principle in nereids, a single hormone, which is

produced most probably in neurosecretory cells of the brain, controls postlarval development in a concentration

dependant manner. It has been found to be neither species specific nor sex specific, and to work in species with and

without epitokous reproductive form.

The present report considers currently available data on the regulation of endocrine activity in Platynereis

dumerilii, one of the most thoroughly investigated nereid species. The following question is asked: is die brain

hormone titer regulated by brain-autonomous control of production and release, or is it determined by a more

complex system ol exogenous and endogenous factors acting on die neurosecretory ganglia? In particular, I review

results of investigations aimed at demonstraung feed-back phenomena during male and female gametogenesis,

metamorphosis and regeneration of posterior segments. These findings are discussed and compared widi studies

bearing on feed-back control in P. cultrifera and on brain-body interaction in Nereis diversicolor (e.g. PORCHET &

Cardon, 1976; PORCHET, 1984; Golding, 1987).

DEVELOPMENT OF PLATYNEREIS DUMERILII

P. dumerilii , originally described from die Mediterranean and the french Atlantic coast, is a gonochoric,

typically monotelic species, which develops a pelagic, epitokous reproductive form. Sex appears to be genetically

controlled and die diploid complement of chromosomes was found to be 28 (Hanske, 1989). The same diploid

chromosome number was found also in the sibling species P. massiliensis and P. megalops (D. JOrg, Univ.

Mainz, pers. comm.). In neither sex are typical gonads present, gametogenesis proceeds in the coelomic fluid.

Recently. Hanske (1989) detected paired, segmental sites at dorsolateral positions, from which small clusters of

spermatogonia appear to be proliferated and released into the coelom (but see die findings in Nereis grubei by

Reish, 1954). Metamorphosis into the reproductive form parallels die final stages of gamete development; die

pelagic heteronereis then broadcasts die fully mature eggs and sperm during pheromone controlled nuptial dances

Source : MNHN. Paris

FEED-BACK REGULATION IN PIATYNEREIS DUMERIIJI

67

(ZEEK et al., 1988 for review). There is no brood protection; early phases of development, including trochophore

and metatrochophore stages, are pelagic. Nectochaeta larvae later start settling and forming tubes on the substratum

from secretions of parapodial glands. In laboratory cultures maintained by now standard methods (HAUENSCHILD,

1951), development from fertilized egg to the heteronereis stage is variable and takes from 3 to 12 months with a

small proportion of "stragglers" taking up to 18 months (HAUENSCHILD, 1966). Of a total of 635 males 65%

reached maturity within 4-8 months (Hanske, 1989); die same author recorded a similar life-span for females.

With its very short life-cycle, correlated widi rapid growth and fast regeneration, P. dumerilii differs considerably

from P. cultrifera and Nereis diversicolor which require 2-3 years to reach ihe reproducuve status in the field.

ENDOCRINE CONTROL OF POSTLARVAL DEVELOPMENT

Results of the pioneer work by DURCHON (1948, 1952), performed first on male Nereis irrorata and Perinereis

cultrifera, suggested that spermatogenesis and epitokous metamorphosis are controlled by an inhibitory, endocrine

factor formed widiin the prostomium. Using female worms, HAUENSCHILD (1956, 1965, 1966) conducted

prostomium amputation experiments on laboratory reared P. dumerilii , focussing on gametogenesis,

metamorphosis and caudal regeneration. His results largely confirmed Durchon's observations, but moreover,

provided a much more detailed hypothesis of the hormonal control mechanism in this species. He concluded that a

single prostomial hormone is responsible for die control of both gametic and somatic development, acting in a

concentration dependent manner. The juvenile growth phase and proliferation of germ cells require a high tiler of

hormone, which inhibits late stages of gametogenesis and epitokous transformations. When oocytes reach

diameters of 80-100 |im, a photoperiodically triggered decrease of hormone concentration initiates a new phase of

oocyte growth and differentiation, stops die addition of new segments, quenches posterior regeneration, and allows

then metamorphosis of somatic tissues. Once die level approaches zero, development of heteronereid swimming

setae is completed and oocytes undergo final maturation. The hetcroncreis then aquires the competence to respond

to sex pheromones, i.e. to perform nuptial dances and to shed the gametes soon after it begins to swim. Since

absolute hormone concentradons could not be measured, HAUENSCHILD (1965) used arbitrary units and suggested,

but did not indicate in his Fig. 19, a logarithmic scale. DURCHON & PORCHET (1971), PORCHET (1973), and

SCHROEDER et al. (1977) arrived at similar conclusions when studying developing individuals of several species

of nereids, despite die fact dial the former audiors were using an entirely different organ-culture system to assay die

hormonal activity of homogenized pros tom ia (sec BERTOUT, 1984 for details of the N. diversicolor

spermatogenesis assay).

The major drawback of the work discussed herein is that die precise site of production and release of the

hormone, its molecular structure, its rate of synthesis and secretion, and its absolute concentrations are not yet

known. We must use live prostomia, or homogenates (fresh or lyophilized) as a source of the active compound,

and we have to deduce or to determine indirccdy relative values of hormone activity (or concentrations respectively)

from biological assays based on morphogenic or cytomorphologic criteria.

All recent evidence confirms die view- diat the hormone concentration in Platynereis dumerilii is maximal in

juvenile animals and decreases to zero in die heteronereid, and a high level of activity is required to sustain

segment formation, to support the proliferation of oogonia and spermatogonia, and to suppress premature

maturation and epitoky (Hofmann, 1975, 1976: Schiedges, 1981; Hofmann & Schiedges, 1984; Meisel,

1990). It has been confirmed diat growdi and regeneration capacity decrease and somatic metamorphosis starts

when die hormone level is lowered. However is has become a matter of dispute whether all successive

developmental events in somatic tissues and germ cells are directly controlled by specific levels of hormonal

activity. HAUENSCHILD (1966) found that oocytes, which, had a critical diameter of about 100 |im, completed a

morphologically normal oogenesis after the prostomium had been removed. No further hormone supply was

required at that stage. On the other hand, implantation of one or two prostomia from juveniles into female

recipients with oocytes of diameters larger than 100 |im significantly prolonged die time of survival, but retarded

and disturbed both oogenesis and metamorphosis when compared to eidier decapitated worms or controls. Though

oocyte development beyond the critical stage can proceed widiout continued hormone secretion, the maturing

oocytes are still sensitive to altered endocrine conditions (Hofmann, 1975).

The same type of experiments led to different results when performed on males. Prostomial removal from

juveniles caused defective development at the end of which die worm fragments were still lacking major

heteronereid characters and did not contain any gametes. Individuals with some small clusters of spermatogonia in

die coelom (early spermatogonia cluster I phase) showed a dual response. Whereas metamorphosis was defective in

68

D.K. HOFMANN

all cases, the course of spermatogenesis was morphologically normal. None of the stages was omitted but the

entire sequence was accelerated : it took only 12.5 days on the average instead of one to several months to produce

mature spermatozoa. If, however, worms were decapitated at the end of the first mitotic proliferation phase (late

spermatogonia cluster I phase), not only spermatogenesis but also metamorphosis was accelerated. At this stage

93% of tiie experimental worms developed normal heteronereid characters (MEISEL, 1990).

Implantation of one to three prostomia from juvenile donors into developing males, from the advanced

spermatogonia cluster stage onward, left spermatogenesis unaffected. Differentiation of sperm proceeded at about

the normal rate. This is in obvious contrast to the findings in females. On die other hand, heteronereid

transformation was strongly affected and disordered by this manipulation of the hormone level, as in the

corresponding experiments on female P. dumerilii (SCHIEDGES, 1981: Hofmann & Schif.dges, 1984).

Gamete development in both sexes and metamorphic events appear to be strictly coordinated in ontogenesis,

but to be experimentally dissociable. Spermatogenesis turns out to be considerably less sensitive to the alteration

of endocrine conditions than oogenesis. It is remarkable that development of heteronereid characters can be

seriously delayed and disturbed by manipulating the endocrine status even very late in gametogenesis. The sibling

species P. massiliensis , although morphologically indistinguishable from P. dumerilii , has an entirely different,

benthic mode of reproduction. These proterandric hermaphrodites do not metamorphose: they deposit, fertilize, and

brood the eggs within their tubes. Posterior regeneration was shown to decrease drastically in die absence of the

prostomium (Casanova, 1955), but no unequivocal proof of brain hormone control of either spermatogenesis or

oogenesis could be developed (Hauenschild, 1970; LOcht, 1987 for review).

FACTORS AFFECTING THE ENDOCRINE ACTIVITY OF THE BRAIN

ENVIRONMENTAL FACTORS

Hauenschild (1966) demonstrated photoperodic control of swarming periodicity in P. dumerilii and has

further shown maturation and epitoky to be hormonally governed. He therefore postulated that the synodic or

experimentally modified light-dark regime acts via the neuroendocrine pathway. However, no detailed study on

light-to-hormone signal conversion is available to prove this hypothesis.

Temperature has been reported to affect hormone gamete-interaction in N. diversicolor (Durchon & Porchet,

1971), but the influence of temperature on development and endocrine activity has not been studied in

P. dumerilii.

REGENERATION OF POSTERIOR SEGMENTS

The number of setigers regenerated following amputation of the posterior end is positively correlated with the

number of segments removed. As mentioned earlier, at a given level of transection, the number of segments

regenerated decreases concomitantly with the progress of gamete maturation and metamorphosis (Hauenschild,

1966: Hofmann, 1966; Schiedges, 1981; Hofmann & Schiedges, 1984). Hauenschild (1966) also noticed

that in maturing females amputation of a significant number of posterior segments led not only to regeneration

but also to retardation of sexual development and to delayed metamorphosis. These results suggest that hormone

production has been stimulated, possibly mediated by the injury of the ventral nerve cord (see Hofmann. 1966 for

discussion of earlier work). More detailed investigations in female P. dumerilii showed that maturation was

delayed and significant regeneration occurred only when about 50 of approximately 70 parapodial segments were

removed. Furthermore, the size of the regenerate and the delay in reaching the heteronereis stage decreased as

individuals of more advanced stages of sexual development were assayed (Hofmann, 1975).

In males, the number of segments regenerated and the delay in heteronereid metamorphosis are likewise

correlated with the number of segments amputated and with die stage of sexual development. However,

spermatogenesis continued unaffected when males from the late spermatogonia! stage onward were assayed. In such

cases we observed males deprived of all but 20 segments which showed posterior regeneration and significant delay

ot metamorphosis, but in which spermatogenesis proceeded independently. They contained mature spermatozoa a

full diree weeks before reaching the heteronereis stage.

I he hypodiesis that the site ot nerve cord lesion causes a position-dependent increase in hormone production

and thus determines the course of regeneration and maturation was tested. In males and females at selected stages of

development, the ventral nerve cord was excised from segments 20 and 21 (or the circumoesophageal connectives

Source : MNHN , Paris

FEED-BACK REGULATION IN PLATYNEREIS DUMERILII

69

deleted) prior to amputation of the posterior end behind segment 40 (Hofmann, 1966, 1975; Schiedges. 1981).

File results did not support the assumption that nerve cord injury activates hormone secretion and thus enhances

posterior regeneration accordingly. Therefore, stimulation of the neurosecretory cells via the nervous system does

not appear to be the decisive control mechanism. There must be other components modulating brain hormone

activity by stimulating its production or by temporarily preventing its decrease. Candidates are die developing

gametes, the somatic coelomocytes interspersed with the gametes, and various somatic tissues.

FEED-BACK ACTIVITY OF GAMETES AND COELOMOCYTES

When deprived of all but 20 segments, female P. dumerilii with oocytes measuring 130- 150 pm in diameter

regenerated up to 12 segments and survived up to 25 days, whereas those cut behind segment 40 did not form

regenerates but transformed into heteronereids within one week, as did the controls. Amputation of about 2/3 of

the animals parapodial segments means dial die hormone "source" has to serve thereafter only a much smaller part

of its "sink". Even at a given, constant production of the factor, a higher concentration may result in the much

smaller body and could account for enhanced regeneration and retarded heteronereid development. If one bears in

mind that some cells of die "sink" acquire the ability to feed back on and to inhibit the hormone producing cells,

cutting off segments involves not only a decrease of the "sink" volume, but also a reduction of die mass of cells

feeding back on die hormone source.

DURCHON (1952) suggested that a coelomic factor associated with the oocytes and clcocytcs of submature

P. cultrifera reduced the endocrine activity of die brain in immature recipients injected with gametocytes and

coelomocytes.

Several lines of evidence indicate dial down-regulating factor(s) exist in P. dumerilii as and are major

components of developmental control (Hofmann, 1975: Schiedges, 1981; Hofmann & Schiedges, 1984;

MEISEL, 1990). In these investigations, the number of segments regenerated by males and females at selected

stages of development, the time period required to form the heteronereis, or the survival time, were used to

determine such effects.

REMOVAL AND INJECTION OF COELOMIC CONTENTS

Removal of oocytes and coelomocytes by stripping following caudal amputation led to enhanced regeneration

and to significantly delayed metamorphosis at stages in which regeneration had normally ceased (HOFMANN,

1975). When intact juvenile worms were deprived of all but 40 segments and were injected with the coelomic

contents of females with oocytes ranging from 100 to 180 pin in diameter, effects on the recipient's development

were observed only when 100 to 120 pm oocytes were injected. Seven out of 15 juvenile recipients started to

regenerate but then stopped and transformed into heteronereis within 1 1 to 17 days, whereas controls took one to

several months (HOFMANN, 1975).

Stripping of gonia from males was much more difficult and could not be done quantitatively. The

experimentals were apparently affected by the manipulation and did not develop well. This will not be considered

further (Schiedges, 1981). Injection of mature spermatozoa and coelomocytes into very young females (oocyte

cluster stage) caused accelerated oocyte growth and metamorphosis, and significantly reduced the regeneration of

posterior segments. Quite unexpectedly, males at the initial stage of gametogenesis did not respond to sperm

injection. On the other hand, juvenile worms, when injected with gonia from spermatocyte/tetrad or tetrad stage

donors, metamorphosed much faster than the controls, i.e. in only about 62 % of the time. However regeneration

was clearly reduced only when the colomic contents of tetrad stage donors was transferred (Schiedges, 1981).

These observations are compatible with the hypothesis that factors, probably stage specific, are associated with

gametes and coelomocytes, which influence development by altering the endocrine activity of die brain. Under

these premises stripping of the oocytes means removal of the feed-back factor and results in hormone production

and, consequently, in enhanced regeneration and delayed metamorphosis. On the other hand, injection of

differentiating gametes and coelomocytes adds such factors which then suppress hormone production in the

immature host. This would account for their limited regeneration and accelerated epitokous development and

maturation.

70

D.K. HOFMANN

PROSTOMIUM TRANSFER EXPERIMENTS

Additional evidence for the existence of coelomic factors which feed back on hormone production has been

provided by prostomium transfer assays. Hauenschild (1966) found that prostomia taken from maturing females

and implanted into decapitated fragments of younger females, exhibited a stronger maturation inhibiting and

regeneration promoting activity than they would have in situ. He assumed that the different "environment" in the

younger recipients had somehow stimulated the activity of the implant. Schiedges (1981) systematically tested

the properties of prostomia taken from males at different spermatogenetic stages and transferred to juvenile,

decapitated hosts. She noticed that prostomia excised from worms at the spermatocyte cluster stage, the

spermatocyte/tetrad stage and at the tetrad stage could be assigned a higher endocrine activity than when tested in

situ , thus confirming and extending HAUENSCHiLD's result.

Schiedges (1981) provided further support through very elegant prostomium passaging experiments performed

on P. dumerilii. Prostomia excised from immature donors were implanted into male intermediate hosts at different

stages of spermatogenesis and were left there for one week. Then die prostomia were excised again and implanted

into definitive, immature, decerebrate 40 segment host fragments.

In individuals receiving prostomia which had been passaged in intermediate hosts ranging from the juvenile

state to die spermatocyte /tetrad stage there was a slight decline in botli numbers of segments regenerated and in

survival time, compared to die controls. However a significant decrease occured only in Uiose receiving prostomia

which had been passaged through intermediate hosts at the tetrad or sperm stage. This proved that die secretory

activity of prostomia is negatively affected when exposed to the coelomic "environment" of maturing males. This

influence appears to be stage dependent and to be strongest during the last two spermatogenic stages. Isolation and

characterization of factors which exert negative feed-back on endocrine acuvity and which do not appear to be sex

specific, has not yet been attempted in P. dumerilii.

FEED-BACK CONTROL OF BRAIN HORMONE ACTIVITY

IN OTHER NEREID POLYCHAETES

Extending DURCHON’s (1952) earlier work, PORCHET (1967), Porchet & DURCHON (1968). and PORCHET &

Cardon (1972, 1976) studied the effect of maturing oocytes ("ovocytes submatures", diameter > 180 pm)

injected with their adhering coelomocyles into recipient male and female worms at different stages of development

in P. cultrifera. In this species, which takes three years to reach sexual maturity, oocyte transfer turned out to

cause long-term effects, observed only after many weeks or even months. Injection of submature oocytes into

juvenile hosts led to precocious gametogenesis: 93 % of die males produced sperm and also transformed into

heteronereids within 110 days. Surprisingly, female recipients underwent only abortive, although accelerated

oogenesis but did not metamorphose, in contrast to the findings in P. dumerili (Hofmann, 1975; Schiedges,

1981; Hofmann & Schiedges, 1984). Injection of coelomic contents was also found to affect posterior

regeneration, i.e. the number of segments regenerated was negatively correlated with the size of the injected

oocytes. Alter carrying submature oocytes for 50 days, initially juvenile recipients failed to regenerate any

segments within a period of 20 days, though controls regenerated an average of 14 segments.

PORCHET & Cardon (1972, 1976) showed that the precocious gametogenesis, epitoky, and inhibition of

regeneration, which followed injection of submature oocytes, was not a response to the injection. They

demonstrated that the eflect is based on a chemical factor, the action of which could only be interpreted in terms of

down-regulation of brain hormone activity in the recipient. In separate assays, they examined the biological effect

of oocytes, coelomocytes, coelomic fluid, and of extracts of somatic tissues on host animals. They found that the

factor causing brain hormone inactivation is associated exclusively with the oocyte fraction. PORCHET & Cardon

(1976) purified the factor from an aqueous cthanolic oocyte extract. The compound appears to be a low molecular

weight substance which is dialysable, heat labile, resistant to proteolytic enzyme action, and ninhydrine positive.

It does not seem to be a peptide, but has been suspected to be a glycoprotein. The feed-back substance is obviously

different from die two peptides, Bj and B2, also isolated from the coelomic fluid of P. cultrifera , which stimulate

the final phase of oocyte differentiation (Porchet al.y 1979).

Golding (1967, 1983, 1985, 1987) provided a large body of evidence for humoral brain-body interaction in

N. diversicolor which corroborates many of the findings and conclusions reported above. N. diversicolor reaches

maturity in the second or third year ol life. It does not develop a pelagic heteronereis but shows an atokous,

benthic reproductive form. Gamete maturation is accompanied by the progressive loss of capacity to proliferate and

Source : MNHN. Paris

FEED-BACK REGULATION IN PIATYNEREIS DUMERIUI

71

regenerate posterior segments. As in the other nereid species considered here, decreasing brain hormone levels

account for this developmental pattern.

Prostomium passaging experiments involving prostomia from female donors at various stages of oogenesis

and using both immature and maturing intermediate hosts, demonstrated that the endocrine activity can be

influenced in either direction. Prostomia from maturing donors, known to exhibit only reduced regeneration

promoting activity, were apparently reactivated when subjected to repeated intracoelomic conditioning in immature

intermediate hosts. On the other hand, deactivation of prostomia was observed after passaging for a prolonged time

period in maturing hosts. Deactivation was readily achieved in prostomia excised from donors at later oogenetic

stages, but failed to occur in some of those taken from juvenile worms. Furthermore, injection of submature

oocytes into immature N. diversicolor had a long-term negative effect on regeneration, provided that the injected

oocytes did not degenerate. However Final oocyte maturation and spawning was not normally observed in these

individuals. Thus, submature oocytes can be assigned a brain hormone deactivating influence in N. diversicolor ,

too.

The results of the prostomium passaging experiments can be interpreted, as proposed in Platy nereis dumerilii,

in terms of inhibition and activation of neuroendocrine activity of the respective prostomia, (hough no information

is available on the regulatory mechanism. Although humoral retroaction on brain hormone activity has been

demonstrated also in male P. dumerilii (SCHIEDGES, 1981: HOFMANN & Schi EDGES, 1984), no corresponding

investigations seem to have been done on male P. cultrifera or Nereis diversicolor. Feed-back control in oogenesis

of Cirratulus cirratus (Olive, 1973) and in spermatogenesis of Arenicola marina (Howie, 1984 for review) are

well-known examples of retroaction in gametogencsis of polychaetes. They are not related, however, to the system

of gamete-brain-soma interaction discussed here for members of the family Nereidae.

ACKNOWLEDGEMENTS

I am indebted to J. Fleck for reading and commenting upon the manuscript. The valuable advice of an

anonymous referee and of D.J. REIS IT is gratefully acknowledged.

REFERENCES

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115-122.

Casanova, R., 1955. — Influence du prostomium sur la regeneration caudale de Platynereis rnassiliensis. C.R. hebd.

Acad. Sci. (Paris). 241 : 1814-1816.

DURCHON, M.. 1948. — Epitoquie experimentale chcz deux polychetes : Perinereis cultrifera et Nereis irrorata. C. R.

hebd. Acad. Sci. (Paris). 227 : 157-158.

DURCHON, M.. 1952. — Recherches experimentales sur deux aspects de la reproduction chez les Annelides Polychetes:

l’epitoquie el la stolonisation. Ann. Sc. Nat. ( Zool . Biol, anirn.) Ser. XI. 14 : 119-206.

DURCHON. M. & M. PORCHET, 1971. — Premieres donnees quantitatives sur 1’activite endocrine du cerveau des Nereidiens

au cours de leur cycle vital. Gen. comp. Endrocinol.. 16 : 555-565.

GOLDING, D. W., 1967. Endocrinology, regeneration and maturation in Nereis. Biol. Bull. (Woods Hole), 133 : 567-

577.

Golding, D. W. . 1983. — Endocrine programmed development and reproduction in Nereis. Gen. Comp. Endocrinol..

52 : 456-466.

Golding, D. W., 1985. — Brain-body interactions in Nereis. Reactivation of the cerebral neuroendocrine system by

endocrine manipulation. Int. J. Invert. Reprod. & Devel.. 8 : 51-59.

GOLDING, D. W.. 1987. — Brain-body interactions in Nereis. Deactivation of the cerebral neuroendocrine system by

ganglion transplantation. Int. J. Invert. Reprod. & Devel.. 12 : 281-294.

Hanske, M.. 1989. — Gametogenese eines monotelischen Anneliden: Beobacht ungen zur Gonienherkunft, zum Verlauf

und zur Feinstruktur der Spermalogenese bei Platynereis dumerilii (Annelida: Polychaeta). Doctoral Dissertation.

Ruhr-University, Bochum. 104 pp.

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HAUENSCHILD. C., 1951. Nachwcis der sog. atoken Geschlechtsform des Polychaeten Platynereis dumerilii (Aud. &

Milnc-Edw.) als eigene An auf Grund von Zuchlversuchen. Zool. Jb. Physiol.. 63 : 107-128.

HAUENSCHILD, C.. 1956. Hormonalc Ilcmmung der Geschlechtsreife und Metamorphose bei dem Polychaeten

Platynereis dumerilii. Z. Naturf '., Jib : 610-611.

Hauenschild. C.. 1965. — Hormone bei Nereiden und anderen niederen Wirbellosen. Zool. Jb. Physiol.. 71 : 511-544.

HAUENSCHILD, C.. 1966. — Der hormonelle EinfluB des Gehirns auf die sexuelle Entwicklung bei dem Polychaeten

Platynereis dumerilii. Gen. Comp. Endocrinol .. 6 : 26-73.

Hauenschild, C., 1970. Bezichungcn zwischen Gehirnhormon und Geschlcchtsdifferenzierung beidem

proterandrischen Polychaeten Platynereis massiliensis. Zool. Anz.. Suppl. Bd.. 33 : 249-253.

HOFMANN, D.K.. 1966. — Untersuchungen zur Regeneration des Hinterendes bei Platynereis dumerilii (Audouin & Milne-

Edwards) (Annelida, Polychaeta). Zool. Jb. Physiol.. 72 : 374-430.

HOFMANN. D.K., 1975. Analysis of the relationship between regeneration, maturation and endocrine system in the

polychaete Platynereis dumerilii. Verb. Dtsch. Zool. Ges. Bochum 1974, Gustav Fischer Verlag. Stuttgart: 314-319.

HOFMANN, D.K., 1976. Regeneration and endocrinology in the polychaete Platynereis dumerilii. Wilhelm Roux' Arch.

Devel. Biol.. 180 : 47-71.

HOFMANN. D.K. & I. Schiedges, 1984. Brain hormone levels and feed-back regulation during gametogenesis,

metamorphosis and regeneration in Platynereis dumerilii - An experimental approach. Fortschr. Zool.. 29 : 73-79.

HOWIE, D.I.D., 1984. — The reproductive biology of the lugworm. Arenicola marina. Fortschr. Zool.. 29 : 247-263.

LOcilT, J.. 1987. — ExperimenteUe und morphologische Untersuchungen zur Geschlechtsreifung und Fortpjlanzung bei

dem proterandrischen Polychaeten Platynereis massiliensis. Doctoral Dissertation, Freie Universitat, Berlin, 126 pp.

MEISEL. J., 1990. — Zur Hormona Abhdngigkeit der Spermatogenese bei Platynereis dumerilii: Licht-und elektronen-

mikroskopische Befunde sowie experimcntelle Untersuchungen in vivo und in vitro. Doctoral Dissertation, Ruhr-

University Bochum. 166 pp.

Olive. P.J.W., 1973. The regulation of ovary function in Cirratulus cirratus (Polychaeta). Gen. Comp. Endocinol. ,

20 : 1-15.

PORCHET, M., 1967. — Role des ovocytes submatures dans l'arret de l'inhibition cerebrale chez Perinereis cultrifera

Grube. C. R. hebd. Acad. Sci. (Paris). 265 (D) : 1394-1396.

PORCHET. M., 1972. — Variation dc 1‘activite endocrine des cerveaux en fonction de l'espfcce, du sexe et du cycle vital

chez quelque Nereidiens (Annelidcs Polychctes). Gen. Comp. Endocrinol.. 18 : 276-283.

PORCHET, M.. 1984. — Biochemistry of oocyte differentiation in nereids. Fortschr. Zool.. 29 : 207-225.

PORCHET, M. & C. Cardon. 1972. — Regulation de l'activite endocrine cerebrale chez les Nereidae (Annelidas

Polychctes). C. R. hebd. Acad. Sci. (Paris), 275 (D) : 2375-2378.

PORCHET. M. & C. CARDON. 1976. The inhibitory feed-back mechanism coming from oocytes and acting on brain

endocrine activity in Nereis ( Polychaetes, Annelids). Gen. Comp. Endocrinol.. 30 : 378-390 .

PORCHET. M. & M. DURCHON, 1968. — Influence dc la maturite genitale sur la regeneration posterieure, chez Perinereis

cultrifera Grube (Ann<Slide Polychete). C. R. hebd. Acad. Sci. (Paris). 267 (D) : 94-196.

PORCHET. M.. DHAINAUT. A. & F. PORCHET-HENNERE, 1979. — Evidence of coelomic substances inducing genital

maturation in Perinereis cultrifera. Wilhelm Roux' Arch. Devel. Biol., 186 : 129-137.

REISH. D.J.. 1954. — The life history and ecology of the polychaetous annelid Nereis grubei (Kinberg). Occ. Pap. Allan

Hancock Found., 14 : 1-75.

SCHIEDGES. I.. 1981. — Spermatogenese, Metamorphose. Regeneration und deren Beziehung zum neuroendokrinen

System bei Platynereis dumerilii. Doctoral Dissertation. University of Cologne. 94 pp.

SCHROEDER. P.C., E. HOFMANN & K. Wallace, 1977. Posterior regeneration and the endocrine control of postlarval

development in Nereis grubei (Kinberg). In DJ. REISH. & K. FAUCHALD (eds.), Olga Hartman Memorial Volume.

Special Pub!. Allan Hancock Foundation. Los Angeles, Calif. : 391-405.

Zeeck. E., IlARDEGE, J.. Bartf.ls-Hardege, II & G. Wesselmann, 1988. — Sex pheromone in a marine polychaete:

Determination of the chemical structure. J. exp. Zool.. 246 : 285 -292.

Source : MNHN. Paris

7

Bioaccumulation du fer dans le corps cardiaque

de Raricirrus beryli Petersen & George

(Polychaeta, Ctenodrilidae)

Jean VOVELLE* Man ’ E . PETERSEN ** Michele GRASSET *

<£ Patricia BEAUNIER ***

*Laboratoire d'Mistologie ct Cytologic des In vertebras Marins

Universite P. ct M. Curie

12. rue Cuvier, F-75005 Paris, France

**Zoological Museum, University of Copenhagen

Universitctsparken 15, DK-2100 Copenhagen 0, Denmark

*** Service de Microscopie electronique GRMP

Universite P. el M. Curie

6, rue Cuvier, F-75005 Paris, France

RESUME

Raricirrus beryli , loealement abondant dans les champs petroliferes de la merdu Nord septentrionale. est reconn u comme

une especc indicatrice pour les sediments pollues par les hydrocarbures. Le materiel provient de deux recoltes : a proximite

nord de la Beryl Platform (mai 1982) et a 200 m nord du premier site (mai 1985). Sa conservation a permis d'entreprenclre une

etude microanalytique (au moyen de la microsonde en dispersion de longueur d'onde, du microanalyseur ionique et de la

microsonde en dispersion d'energie) et d'obtenir des indications sur sa structure cytologique. L'organe etudie est le corps

cardiaque. dont le role possible de detoxification peut se traduire par des differences entre les specimens des deux recoltes. Les

elements detectes par la microanalyse sont surtout le fer. et en quantites moindres du calcium, soufre, phosphore et aluminium.

Les autres elements rcperables sont le magnesium, le chlore, des traces de cuivre, de vanadium et de fluor ; zinc et silice sont

absents. Le fer a cte identifie a 1'echelle ultrastructurale sous la forme de particules intracytoplasmiques de ferritine,

concentrees souvent dans des inclusions delimitees par une membrane ou intdgrdes a des granules spherulaires. La difference

entre les deux recoltes se manifesto dans la teneur en fer, trois fois plus forte dans les specimens a proximite de la plateforme.

Chez quelques uns d'entre eux. le fer apparait a 1'echelle ulUastructurale comme un feutrage d’aiguilles entourant certaincs

spherules. Cette surcharge complique la fonction hematopoietique supposee du corps cardiaque, on suggere qu'elle joue un role

dans la detoxification.

ABSTRACT

Iron bioaccuimilation in the heart body of Raricirrus beryli Petersen & George (Polychaeta, Ctenodrilidae)

VovELLE, J.. PETERSEN, M.E., GRASSET. M. & P. BEAUNIER, 1994.- Bioaccumulation du fer dans le corps cardiaque de

Raricirrus beryli Petersen & George (Polychaeta, Ctenodrilidae). In: J.-C. DAUVIN. L. LaUBIER & D.J. REISH (Eds), Actes de

la 4eme Conference intern ationale des Polychetes. Mem. Mus. nain . Hist. nat.. 162 : 73-80. Paris ISBN 2-85653-214-4.

Source : MNHN , Paris

74

J. VOVELLE, M.E. PETERSEN. M. GRASSET & P. BEAUNIER

Raricirrus beryli , which is abundant in the oilfields of the northern North Sea. has been recognised as an indicator species for

hydrocarbon-polluted sediments. The material came from two different sites in the North Sea: one just north of the Beryl

platform May 1982). the other 200 meters north or the platform (May 1985). A microanalytical study was earned out using a

wavelength X-ray spectrometry microprobe, an ion microanalyser, and an energy dispersive spectrometry microprobe. The

cytological structure of the dorsal heart body was studied from sections embedded in araldite. The elements detected under

microanalysis were mainly iron and small amounts of calcium, sulfur, phosphorus, aluminium, magnesium, chlorine, copper,

vanadium and fluorine. Neither zinc nor silica were detected. Iron was identified as a form of inlracytoplasmic ferritin particles

which were concentrated in membrane-bound inclusions or integrated with spherular granules. The main difference between

the two sites was in the amount of iron, which was three times greater in specimens close to the platform as in those from 200

meters. Iron was detected at the ultrastructural level in the form of needles surrounding some of the spherules from some

specimens collected near the platform. This overload of iron is not in keeping with the supposed haematopoietic function of the

heart body, it is hypothezed that it plays a part in the detoxification process.

INTRODUCTION

L'animal retenu pour cette dtude, Raricirrus beryli, a 6t6 ddcrit en 1991 (Petersen & George, 1991) et

reconnu comme une nouvelle esp£ce de polych&te indicatrice pour les sediments polluSs par les hydrocarbures

(Moore, 1991). Les dchantillons qui out permis notre recherche out recucillis dans deux sites diffdrents : l'un

a proximity de la plateforme pdtroli&re Beryl dans la mer du Nord, l'autre 200 m plus loin. Meme si l’dcari de

temps qui sdparc les deux rdcoltes relativise la rigueur de nos conclusions, la difference d’aspect des corps

cardiaques des animaux dans les deux rdcoltes impose l'hypoth£se de leur intervention dans un processus de

detoxification. Leur conservation ne permettait pas d'envisager une etude cytologique fine, mais du moins

l'appreciation de differences significatives dans leur composition eiementaire, par les methodes de la microanalyse

k rechelle structural et ultrastructurale.

L'interpretation du corps cardiaque present chez cinq families de Polychetes a fait I’objet de nombreux travaux.

Si 1'on admet maintenant son homologie avec le tissu chloragogene "extravasal" qu'on trouve dans d’autres

families, on sait aussi que ce dernier a pu etre decrit comme un rein d'accumulation avant qu'on examine son role

dans l'h&natopoifcse. La priorite de cette fonction est dorenavant acceptee aussi bien pour le corps cardiaque que

pour le tissu chloragogene, mais son intervention peut interesser aussi bien la degradation et peut-etre le recyclage

du pigment respiratoire que sa biosynthese. A cote de 1'accumulation de produits accessoires decrite par Kennedy

& Dales (1958) comme le resultat du catabolisme des metalloporphyrines, l'intervention possible des corps

cardiaques dans des processus de detoxification a ete evoquee dans leur potentiality de sequestration d'eiements

exogenes figures ou non (Braunbeck & Dales, 1984). Enfin, dans les incertitudes meme de son utilisation, le

concept de "chloragosome" prend en compte dans les travaux r6cents (Ouaghi & GRASSET, 1991) une possibilite

de bioaccumulation progressive notamment du fer. Une telle bioaccumulation pourrait-elle etre l'indice indirect

d'un etat physiologique modifie par la surcharge environnementale en hydrocarbures? A travers l'hypoth&se d'une

detoxification chez une espece priviiegiee, e'est done aussi k l'interpretation du role du corps cardiaque en

conditions normales que notre travail tente de contribuer.

MATERIEL ET METHODES

Le materiel utilise pour cette etude provient de deux recoltes differentes. Tune et 1'auire de la mer du Nord

septentrionale : l'une pr£Iev6e juste au nord ("close up N" = CU N) de la plateforme petrolifcre Beryl (mai 1982),

l'autre 200 metres au nord (200 N) du point precedent (mai 1985). Les animaux ont ete fixes au formol k 10 % et

le preievement CU N a ete ensuite transfere dans l'alcool ethylique k 80 °C.

Les specimens examines ont ete tromjonnes au niveau du corps cardiaque (au deD du 9e s6tigere) et inclus

dans l'araldite apres deshydratation k l'alcool. L'anatomie microscopique a ete etablie sur coupes transversales

Fig. 1. A. Region dorsale (specimen 15, CU N). Coupe transversale semi-fine coloree au bleu de Toluidine (barre 50 pm);

v : espace sanguin ; B. Detail du corps cardiaque (specimenl3, 200 N), meme preparation (barre 10 pm) ; C, D, E, F.

Micrographies electroniques sans post-osmication ni coloration (barre 200 nm pour C et E. 100 nm pour D et F) ; C.

Spherule entouree d’aiguillcs d'oxyde de fer (specimen 1 8 CU N). D. Granule de ferritine (specimen 5, 200 N), E. Spherule

homogene enrichie supcrficiellement en ferritine (specimen 4, 200 N), F. Particules intracytoplasmiques de ferritine

(spdcimenl8, CU N), G. Images d’emission ionique (sp6cimenl5, CU N). 27+ : Al. 40+ : Ca, 56+ : CaO + Fe (meme

echelle que A).

Source : MNHN. Paris

BIO ACC U M U L. ATION DU FER CHEZ RARICIRRUS BERYU

75

Source ; MNHN, Paris

76

J. VOVELLE, M.E. PETERSEN. M. GRASSET & P. BEAUNIER

semi-fines colonies au bleu de toluidine, l'fetude cytologique ultrasiructurale sur coupes ultra-fines non colorfees.

La fixation initiale et le mode de conservation du materiel ne pouvaient permettre qu'une approche grossifere des

ultrastructures, excluant toute post-osmication et toute identification des organites et des membranes.

L'fetude microanalytiquc a fait appel b trois instruments diffferents.

- sur coupes semi-fines, aprfes montage sur terphane carbon6, microsonde MS 46 Cameca fequipfee dc

spectrographes dispersifs en longueur d’onde b cristaux K AP et PET (diamfetre de sonde 1 pm);

- sur coupes semi-fines fetalfees sur support de platine, microanalyseur ionique Cameca SMI 300 (spectres

acquis sur tout le champ image, diamfetre 260 pm);

- sur coupes ultra-fines montees sur grille de cuivre, microscope felectronique Temscan JEOL JEM CXII

fequipfe d'un d6tecteur de rayons X b selection d'fenergie (EDS) LINK module AN 10000 b cristal SI(LI). Tension

d'accfelferation 60 kV. Surface analysfee pour chaque spectre 50 xlOO nm, temps dc comptage 300 s.

Vingt-cinq individus out fetfe examines b l'fechellc photonique (15 pour 200 N. 10 pour CU N), 20 b 1'fechclle

ultrastructurale, 18 en microanalyse par dispersion de longueur d'onde, permettant la selection des quatre retenus

pour la microanalyse par dispersion d'fenergie el des deux 6ludi6s au microanalyseur par Emission ionique

secondaire.

RESULT ATS

L'examen b la loupe des vers provenant des deux rfecoltes permet de reconnaitre le corps cardiaque, dorsal et

visible b travers l'fepithfelium, comme une ligne pigmentfee plus ou moins sinueuse partant du 8 ou 9 feme sfetigfere

et courant sur les 10 a 15 suivants. Brun noiratre, il apparait plus fonefe et plus fepais pour les individus provenant

du lot CU N que pour ceux de 200 N.

anatomie microscopique ET HISTOLOGIE (Fig. 1A-B). — De section circulate en coupe transversale,

l'organe est suspendu entre l'fepiderme ct le tractus digestif par un mfesotlifelium qui se dilate localement pour

former un ou plusieurs vaisseaux. La masse compacte de cellules constituant le corps cardiaque baigne ainsi dans

un espace vasculaire plus ou moins dfeveloppfe, dfelimitfe par une "basale" extracellulaire ("vascular lamina")

supportant exterieurement les corps cellulaires d'un revetement pferitonfeal (myomfesothfelium), et sans doutc

inflfechie pour delimiter le pourtour du corps cardiaque. Cc dernier prfesente en coupe une douzaine de cellules b

noyau x pourvu d'un gros nuclfeole, pferiphferiques p<u‘ rapport b leurs inclusions de taille et de contraste divers,

certaines trfes opaques, d'autres jaunatres et translucides.

Kennedy & Dales (1958) ayant signalfe l'feventualitfe du dfeveloppement du corps cardiaque avec l'age et la

bioaccumulation, nous avons comparfe pour les deux lots de Raricirrus plusieurs systfemes indicateurs.

Les valours obtenues (n= nombre d'individus fetudifes) ne marquent pas de difference significative en ce qui

conceme :

- le diamfetre du corps au niveau examine :

200 N : 251 ± 16 pm, n = 5; CU N : 274 ± 18 pm. n = 7

- le diamfetre du corps cardiaque :

200 N : 35 ± 9 pm, n = 14; CU N : 36 ± 8 pm, n = 11.

L'intfegritfe des cellules est identique dans les deux lots. Le dfeveloppement de l'espace vasculaire pferiphferique

est variable dans les deux lots, peut etre plus souvent important pour CU N. Par contre, on reconnait davantage

d'inclusions Claires pour 200 N.

CYTOLOGIE (Pig. 1C-D-E). — La preparation du materiel b notre disposition ne permet qu'une appreciation

incomplete des ultrastruc lures : les membranes sont rarement identifiables, les noyaux et certains organites

(mitochondries) alteres et on devinc a peine certains trajets canaliculaires intracytoplasmiques. L'absence la plus

regrettable conceme les vacuoles qui doivent concentrer le pigment respiratoire. Ceci acceptfe, on peut faire

l'inventaire et la description dc divers types d'inclusions, plus ou moins contrastfees et dont l'opacitfe aux felectrons

est en partie attribuable b un mfetal prfesent naturcllcmcnt, que la microanalyse dfesignera comme du fer.

La majoritfe des inclusions des cellules du corps cardiaque correspond dans les deux lots b des sphferules rfeguliferes

de diamfetre moyen 0,9 pm (jusqu'ft 1,5 pm) d'un matferiau homogfene modferfement contrastfe, cl la pferiphferie

desquelles on devine parfois une membrane. Elies peuvent etre regroupfees en amas moruliformes (jusqu'a

2,5 pm), parfois cernfees d’une couche externe moins dense el plus souvent, dans les deux lots, d’une zone

contrastfee de particules que nous reconnaitrons comme de la ferritine (Fig. IE). Cette ferriline peut envahir

complfetement la spherule dans une rfepartition regulifere ou localisfee.

Distincts des sphferules par leur contraste et leur diamfetre moyen (0,3 pm. Fig. ID) des amas arrondis de

ferritine. sans apparence de membrane pferiphferique, sont fegalement prfesents dans les deux lots. Les particules

BIO ACCUMULATION DU FLR CHEZ RARICIRRUS BERYL!

77

constitutes sent plus ou meins organises, encore qu'on n'y observe jamais de plages pseudocristallines telles

flu on en connait dans les inclusions comparables du tissu chloragogfene des Sabellidae (Ouaghi 1989) et

Serpulidae ( Vovelle et al. ,199 1 ). On recommit dans les memes cellules des plages plus petites (0,2 urn) et moins

organises des memes particules, assuremem intracytoplasmiques, it contours iruSguliers (Fig. IF). Ces particules

fenitin like pour quelques auteurs (mais que nous confiimerons par la microanalyse) apparaissent isol6ment en

plus ou moins grande density dans l'ensemble du cytoplasme. A grossissement convenable, leur taillc (environ

12 nm) et leur conformation fournissent un nouvel ei&nent ^identification.

Line partie de ces inclusions est comparable <t cellcs d^crites par divers auteurs (i.a. Friedman & Weiss

1980_; Ouagiii & Grasset, 1991) dans les corps cardiaques el tissus chloragogfenes de diverses Polycheles et

peut etre mterprC-tde dans le cycle de l'h6matopoi6se. Les spherules homogenes sont originales et nous hdsitons it

leur donner un rapport de filiation avec les "granules de ferritinc", meme si elles peuvent se charger de particules.

On les distingue en tout cas des inclusions Claires lipidiques it membrane qu’on peut identifier dans quelques

specimens des deux lots. ^

f255c

'X

FIG. 2. — Microanalyse en selection denergie sur coupes ultra fines (specimen 18. CU N) A. Granule de ferritine. B. parlic

centrale dune spherule homogene. C. Feuirage d’aiguilles peripherique a une spherule. Tension d’acceleration 60 kV, temps

de comptage 300 s. En blanc sur les schemas : surface analysce; c : nombre de coups.

78

J. VOVELLE, M.E. PETERSEN. M. GR ASSET & P. BEAUNIER

II appartienl ft deux individus sur neuf examines dans le lot CU N de presenter une surcharge originate des

spherules homogEnes : dans certaines plages cellulaires elles sent recouvertes sur une Epaisseur de 0,1 pm d’un

feutrage d'aiguilles ft fort contraste, alors que leur matiEre fondamentale est souvent chargee de particules de

ferritine (Fig. 1C). Ccs aiguilles de dimension moyenne 50 nm Evoquent celles que nous avons dEcrites en filiation

d'inclusions°de ferritine dans la biominEralisation cuticulaire des machoires d'un Eunicien (VOVELLE et al., 1989)

ou celle que Coulon el al. (1987) ont reconnues dans des conditions de pollution naturelle ft la surface des

filaments de byssus de moules. Ces auteurs y ont identify des oxydes mEtalliques (hematite principalement) et

celte interpretation est ft prendre en compte pour notre materiel.

M1CROANALYSE. — Sped romet vie de rayons X en dispersion de longueur d'onde. On a d'abord examine deux

individus differents dans chacun des lots. Les elements presents ont EtE reconnus et appreci6s ft partir de

moyennes etablies sur une dizaine de points (1 pm environ) particulierement emissifs dans deux ou trois coupes

voisines de chaque echantillon. Ixs elements reconnus sont en ordre d'importance Fe, S, Ca, P, Al et Cu (traces).

La recherche de Zn et V, suggeree par leur existence dans le tissu chloragogEne des Serpulidac, n’a pas domte de

reponse significative. Les valeurs obtenues pour Al ne presentent pas de variation notable entre les deux lots (non

plus que celles de Cu). Les valeurs moyennes concemant les ElEments majeurs ont EtE companies aux valeurs

maximales obtenues pour chaque Echantillon, par rapport auxquclles elles sont minorees dans la proportion d’un

tiers. Si on compare les deux lots, les moyennes pour Ca et P sont majorEes pour le site CU N, et encore plus en ce

qui conceme S et surtout Fe.

Dans un deuxiEme temps on a done apprEciE systEmatiquement, en retenant les memes dEfinitions de valeurs

moyennes, I'intensitE de rEponse du fer, en parallEle avec celle du soufre, pour 9 individus du lot CU N et 7 du lot

200 N. Les valeurs moyennes et maximales pour Fe sont multiplies par trois pour la rEcolte la plus proche de la

station Beryl. Ce ci reprEsente une moyenne de :

CU N : 145 ± 60 c/s (max. 252), contre 200 N : 58 ±31 c/s (max. 89).

En ce qui conceme le soufre, les valeurs obtenues sont :

CU N : 43 ± 17 c/s (max. 58), contre 200 N : 25 ±10 c/s (max. 36).

Le soufre ne prEsente done pas une Evolution aussi marquEe que le fer. Si 1'on compare les valeurs obtenues ft

cedes concernant le tissu chloragogEne et le corps cardiaque des Sabellidae, Serpulidae el Amphictenidae

(Vovelle el al., 1991), elles apparaissent plus faibles, car obtenues sur coupes semi-fines, mais surtout la

participation du phosphore est minorEe, cede du soufre plus importante.

Microanalyse par emission ionique secondaire. Les renseignements exploitEs concement les spectres

d'Emission d'ions secondaires positifs et nEgatifs et les images obtenues pour les ElEments les plus Emissifs. Un

individu de chaque lot a EtE examinE.

Sur les spectres d’Emission les ElEments identifies sont par ordre d'importance Ca (40+), Fe (56+), Al (27+), S

(32-), Cl (35 ) imputable en partie ft la rEsine, P mal servi par la mEthode mais present dans diverses combinaisons

(POCa 87+), Mg (24+) et Cu (63+) comme intervenants mineurs, et F (19 ) en traces. Ces Evaluations intEgrent

l'analyse d'une surface de 200 pm de diamEtre, supErieure ft cede de l'organe en coupe.

L'analyse des images obtenues ft partir des masses prEsentant la meilleure intensitE d'Emission, 56+, 40+, 27+

(Fig. 1G), impose qu'on tienne compte du contraste entre l’organe considErE et les tissus environnants, pour

apprEcier une concentration locale de 1'ElEment identifiE. La masse 56+ imputable ft Fe plus qu'ft CaO prEsente le

meilleur contraste, alors que Ca et surtout Al sont prEscnts dans les autres parses de la coupe.

Meme si la rEponse du fer est meilleure sur l'Echantillon provenant du lot CU N. cede mEthode ne permet pas

d’apprEcier quantitativement des diffErences significalives entre les vers des deux provenances.

Spectrometrie de rayons X en selection d'tnergie. Cct examen ft l’Echelle ultrastructurale sur coupes fines

fournit des spectres correspondants pour les divers types d’inclusions ft des surfaces analysEes de 100 X 50 nm.

Une approximation de 1’importance relative des divers ElEments presents dans chacun d’eux a EtE obtenue pour

deux Echantillons de chaque lot en comparanl r importance des pics obtenus dans des conditions identiques,

exprimEe en coups. Les ElEments reconnus correspondent dans l’ordrc d’importance aux pics Fe, 0, Al, S. P et Ca.

On les identifie dans les accumulations de ferritine, dans les sphErules homogEnes et dans le feutrage d’aiguilles

pEriphErique ft certaines sphErules du lot CU N.

En ce qui conceme le fer, la rEponse maximale est de 35 ± 9 coups dans le cytoplasme, 86 ± 18 et 102 ± 39

coups au centre des sphErules homogEnes claires (200 N et CU N), mais les sphErules chargEes de ferritine

peuvent en prEsenter davantage, 183 ± 36 (200 N) et 155 ± 20 (CU N) dans les amas arrondis de ferritine, jusqu’ft

277 ± 80 dans le feutrage pEriphErique (CU N).

BIOACCUMULATION DU TER CHEZ RARICIRRUS HER YU

79

La presence de l'oxygfene, notable sur les spectres, est contingente du carbonage des grilles. Celle de

l'aluminium est confirmee dans tous les cas, sans indication d'accumulation particulidrc dans les spherules, ni de

difference marquee selon les provenances.

Le rapport du phosphore au soufre est significatif, leurs deux pics sont altemativement preponderants. Le

phosphore est plus important que le soufre dans les accumulations de ferritine, ce qui n'est pas aussi net dans les

feutrages en aiguilles. Le soufre (organique?) a la priori te au centre des inclusions spherulaircs. La presence du

phosphore dans la ferritine est generalement acceptee ; nous interpretons celle du soufre dans les spherules clairs

en rapport avec une composante protdique probable, comportant dcs acides amines soufr6s.

DISCUSSION ET CONCLUSIONS

Les trois methodes de microanalyse utilisees ne concement pas le meme champ dimcnsionnel, l'unc presentam

la repartition des elements dans I'animal. l'autre dans l'organe, la demi&re au niveau uitrastructural dcs inclusions

cellulaires. Leurs performances mais aussi leurs deficiences par rapport k certains elements sc competent. La

convergence des rdsu I tats obtenus permet de proposer un inventaire des elements majeurs concentres par le corps

cardiaque : fer, calcium, soufre et phosphore, les elements mineurs ou traces ne presentam aucun caractere

original. La presence notable de l'aluminium est confirmee par les trois methodes, elle conccrne l'ensemble des

tissus de I'animal sans enrichissement considerable au niveau du corps cardiaque, ni difference marquee entre les

deux sites. S'agit-il d'un element artefactuel, induit par une des manipulations preparatoircs ? II est impossible

actuellement de le d6montrer. Les elements reconnus dans les deux lots de provenance difl'erentc sont identiques.

Ils sont tous interpretables en rapport avec une fonetion hematopoietique de l'organe. La seule donnde apportee

par l'dtude de microanalyse (microsonde MS 46) pour differencier les vers de CU N et de 200 N concerne

I'abondance du fer dans le corps cardiaque dont la valeur triple k proximite de la plateforme, sans qu'aucun autre

element ne presentc une bioaccumulation correlative.

Cette surcharge imputable k un seul metal implique dans le metabolisme du pigment respiratoire est en bon

accord avec deux autres donnees, morphologique et ultrastructurale. Morphologiquement il s'agit de l'indice de

dep;irt, l'intensite de la pigmentation brun noir de l'organe, rcnforc6e pour le lot CU N. A l'echelle ultrastructurale

il s'agit de la presence spedfique dans des individus du meme lot de depots ferriques en aiguilles peripheriques k

certaines inclusions. Cette forme d'accumulation du metal, dont la reversibilite est moins evidente que pour la

ferritine, dvoque une surcharge qu'on peut raisonnablement mettre en rapport avec une h6matopoiese et un cycle

du pigment respiratoire sollicites par les conditions environnementales. Les conditions de conservation des

animaux ne permettent pas de ddcrire davantage la cytophysiologie des corps cardiaques de Raricirrus, qui pourra

etre prdcisde dans une dtude ultdrieure, mais elles nous autorisent ddjh k envisager un rapport entre celle forme

spdcifique de bioaccumulation du fer et un processus de detoxification dcs animaux exposes h un milieu riche en

hydrocarbures.

BIBLIOGRAPHIE

Brauxbeck. T. & DALES, R. P.. 1984. The role of the heart body and of the extravasal tissue in the disposal of foreign cells

in two polychaete annelids. Tissue & Cel! , 16 : 557-563.

COULON, J.. TRUCHET, M. & MaRTOJA, R., 1987. — Chemical features of mussels (Mylilus edulis) in situ exposed to an

effluent of the titanium dioxyde industry. Annls Inst. Octanogr 63 : 89-100.

FRIEDMANN, M.M. & WEISS, L., 1980. An electron microscopy study of hemoglobin synthesis in the marine annelid

Amphitrile ornata (Polychaeta Terebellidae). J. Morphol. , 164 : 121-138.

KENNEDY, G.Y. & Dales, R. P.. 1958. — The function of the heart-body in the Polychactes. J. mar. biol. Ass. U.K.. 37 : 15-

31.

MOORE, D.C., 1991. — Raricirrus beryli Petersen & George (Ctenodrilidae): a new Polychaete indicator species from

hydrocarbon-polluted sediments. Ophelia Suppl., 5 : 447-486.

OUAGHI, E. M., 1989. — Bioaccumulation naturelle du fer chez Sabella pavonina S. (Annelide Polychete). C.R. Acad. Sci.

Paris , 308 : 237-244.

OUAGHI, E. M. & GRASSET. M., 1991. Synthesc et exocytose de chlorocruorine et mise en reserve du fer par le tissu

perivasculaire d'un annelide polychete. Can. J . Zool.. 69 : 2338-2348.

80

J. VOVELLE, M.E. PETERSEN. M. GR ASSET & P. BEAUNIER

PETERSEN, M. E. & George, j. D.. 1991. — a new species of Raricirrus from northern Europe, with notes on its biology and

a discussion of the affinities of the genus (Polychaeta: Ctenodrilidae). Ophelia, Suppl., 5 : 185-208.

VOVELLE. J.. GRASSET. M. & TRUCHET, M., 1989. — Biomineralisation des mac ho ires chez Hyalinoecia lubicola (Muller)

(Polychete. Eunicida). Annls Inst . Ocdanogr.. 65 : 15-36.

VOVELLE, J.. GRASSET. M. & TRUCHET, M., 1991. — Sites of biomineralization in the Polychaete Pomatoceros triqueter

(Serpulidae) with comments on some other species. Ophelia, Suppl.. 5 : 661-667.

Source : MNHN, Paris

8

Functional ciliary groups of the feeding palps

of Spionid polychaetes

Daniel M. DAUER

Department of Biological Sciences

Old Dominion University

Norfolk. Virginia, USA 23529

ABSTRACT

Functional ciliary groups of the feeding palps of spionid polychaetes are reviewed. Six functional ciliary groups have

been observed: frontal cilia, latero-frontal cirri, lateral cilia, ciliated papillae, non-motile cilia of the frontal surface and

basal transverse cilia. The number of functional ciliary groups present on any species varies from one to four groups.

Some ciliary groups, e.g. frontal cilia, are present on the palps of many species while other groups, e.g. basal transverse

cilia, are unique to a single species. Additional studies are necessary to clarify the roles of and possible interactions

between (1) functional ciliary groups. (2) mucus and (3) hydrodynamics in particle encounter, retention, transport and

rejection.

RESUME

Croupes ciliaires fonctionnels des palpes "trophiques" des polychetes Spionidae

Une revision dcs groupes ciliaires fonctionnels des palpes "nutritionnels" des polychetes Spionidae est entreprise.

Six groupes ciliaires fonctionnels ont ete observes : cils frontaux. cirres latero-frontaux, cils lateraux. papilles cilides,

cils non mobiles de la surface frontale et cils transverses frontaux. Le nombre de groupes ciliaires fonctionnels presents

chez chacune des especes varie de un a quatre. Quelques groupes ciliaires. coinme les cils frontaux. sont presents sur les

palpes de beaucoup d’especes tandis que d’autres groupes, comme les cils transverses basaux. ne sont presents que chez une

espece. Des etudes complementaires sont necessaires pour clarifier les roles et les interactions possibles enue (1) groupes

ciliaires fonctionnels, (2) mucus, (3) hydrodynamique dans la rencontre, la retention, le transport et le rcjet des particules.

INTRODUCTION

Spionid polychaetes are common inhabitants of infaunal and epifaunal communities of marine and estuarine

habitats. The ciliated peristomial palps of spionid polychaetes function in (1) feeding behavior (Fauchald &

JUMARS. 1979), (2) inter- and intraspecific interactions (LEVIN. 1981) and (3) tube construction (MORTENSEN &

Galtsoff, 1944). In feeding behavior die palps may function in particle encounter, retention, transport, and

rejection (e.g. Taghon el al., 1980; Dauer et al. , 1981). Spionid polychaetes use their palps to capture particles

in suspension, bedload transport and deposited at the sediment surface; direct deposit feeding using the everted

DAUER. D.M.. 1994. Functional ciliary groups of the feeding palps of Spionid polychaetes. In: J.-C. Dauvin.

L. LauBIER & D.J. REISII (Eds), Actes de la 4eme Conference internationale des Polychetes. Mem. Mus. natn. Hist, run.,

162: 81-84. Paris ISBN 2-85653-214-4.

Source : MNHN. Pans

82

D.M. DAUER

pharynx has also been observed (Daro & Polk, 1973; Wilson, 1983). The potential rapid flux between

suspended, bedload, and deposited stales caused DAUER et al (1981) to classify spionids as interface feeders. In this

paper studies concerning the role of cilia on the palps are reviewed and areas of future research discussed.

DISTRIBUTION OF FUNCTIONAL CILIARY GROUPS WITHIN AND BETWEEN SPECIES

Studies combining feeding behavior and detailed morphological observations have been performed for eight

spionid species and Table 1 summarizes the distribution of ciliary groups among these species. Spionid

polychaetes with a median ciliated food groove have one or more of the following five functional groups of cilia

on their palps: (1) frontal cilia that line the median groove of the palp, (2) latero-frontal cilia organized as

compound cilia (cirri), (3) lateral cilia that beat in metachronal waves, (4) non-motile cirri located at the tips of

papillae, and (S) basal transverse cilia at the base of the palp. Within a species, the number of functional ciliary

groups varies from one to four. For example, Malacoceros indicus has only frontal cilia lining the food groove

(Dauer & Ewing 1991) and Paraprionospio pinnata has four ciliary groups - frontal cilia, latero-frontal cirri,

lateral cilia and basal transverse cilia (Dauer. 1985). Between species, some ciliary groups, e.g. frontal cilia, are

present on the palps of many species while other groups, e.g. basal transverse cilia, are unique to a single species.

Scolelepis squamata and S. hutchingsae lack a median food groove and die cilia of the palps are non-motile and

organized into numerous transverse rows (Dauer, 1983, 1987).

TABLE 1. — Distribution of ciliary groups among the Spionidae.

(from 1- Dauer, 1983; 2- DaUER. 1984; 3- DaUER. 1985; 4 - DaUER, 1987; 5 - Dauer, 1991; 6 - Dauer & Ewing, 1991).

X: ciliary or cirral group is present. — : ciliary or cirral group is absent.

FEEDING BEHAVIOR

The ciliary groups of the palps of spionid polychaetes may function in particle encounter, retention, transport,

and rejection. Particle capture implies particle encounter and subsequent retention. Particle transport implies the

movement from the site of capture to the pharynx. Particle rejection implies that the particle is not ingested after

capture and would include loss during u*ansport as well as transport away from the pharynx.

Particle encounter in the deposit feeding mode occurs as the frontal surface of the palp is placed onto the

sediment surface and can be predicted as a function of panicle size with larger particles having a higher probability

of being encountered (Jumars et ai, 1982). In the suspension feeding mode, particle encounter prediction is a

function of encounter mechanism (direct interception, inertial impaction, gravitational deposition, diffusional

deposition, electrostatic attraction, SHIMETA & Jumars, 1991). The frontal surface of the palp is the site of

particle encounter, but the ciliary groups of Table 1 probably have no role in particle encounter dynamics of

deposit feeding and could only have a role in suspension feeding if currents produced by the cilia of the palps

altered ambient flow conditions. Dauer (1984, 1985) hypothesized that both the latero-frontal cirri and lateral cilia

of P. pinnata and Streblospio benedicti created currents that increased particle encounter during suspension feeding.

Ciliary currents would be functional only in low ambient flows such as in highly deposilional environments or

close to the sediment surface in the bottom boundary layer.

Source :

FUNCTIONAL CILIARY GROUPS OF SPIONID TROPHIC PALPS

83

Retention of particles in spionid polychaetes is assumed to be due to the adhesive properties of mucus secreted

on the frontal surface and the interaction of mucus and surface properties of the particle (roughness, organic

coatings) (Jumars et al. , 1982). Hydrodynamic particle retention, produced by cilia of the palps (sensu Jorgensen

1981, 1982), again could only occur under low ambient flow conditions or when the collection surface is sheltered

from ambient flow (Shitema & Jumars, 1991). Mucus is particularly important in particle retention of the

Scolelepis spp. The non-motile cilia of the Scolelepis spp. were interpreted by Dauer (1983, 1987) as providing a

rough textural surface to retain die particle-mucus complex which was transported to the pharynx by complete

retraction of the palp frontal surface directly onto the pharyngeal surface. Dauer (1987) hypothesized this

mechanism was an adaptation to the highly turbulent habitat occupied by both species and minimized the loss of

particles during transport along die food groove of the palp as envisioned by Self & Jumars (1978). Particle

retention during transport can also be a function of the depth of the food groove. For example, in P. pinnata the

food groove is deep and wide and particles up to 100 pm in greatest dimension were completely enc-losed by the

lateral edges of the frontal surface during transport to the pharynx (Dauer, 1985). Particles less than 100 pm

make of the vast majority of particles ingested by P. pinnata (Dauer, 1980; Luckenbacti et al .. 1988).

Particle transport to die pharynx, as a particle-mucus complex, is primarily accomplished by the beating of the

frontal cilia in those spionids with a median food groove. For the Scolelepis spp. die non-motile cilia of die

frontal surface serve indirectly in particle transport by holding the particle-mucus complex onto die frontal surface

as die palp contracts onto die pharynx (Dauer, 1983).

Frontal cilia may also function in particle rejection from die pharynx by a reversal of the direction of ciliary

How. This mechanism has been observed only in Polydora ligni (Dauer et al., 1981). The basal transverse cilia of

P. pinnata function in particle rejection by die production of a rejection current within die tube. Particles rejected

at the site of the pharynx are rejected into die current produced by the beating of the basal transverse cilia and the

frontal cilia of the branchiae (Dauer, 1985). Dauer (1988) hypothesized that die particle rejection current of

P. pinnata enabled the animal to reject particles at the site of the pharynx while allowing the prostomium to

remain below' the sediment-water interface and thus potentially reducing predation or browsing. In odier spionid

species the everted pharynx is held al the sediment surface or die edge of die lube and particles are rejected directly

onto the sediment-water interface.

The ciliated papillae of spionids do not appear to have any direct function in feeding behavior. Dauer (1991)

hypothesized that the papillae of the palp arc primarily mechanosensory structures that may be important in

interspecific encounters.

The role of the lateral cilia and the latero- frontal cirri is particularly problematic. DAUER (1984, 1985) by

analogy to lamelli branch bivalves and lophophores concluded diat botii ciliary groups functioned in capturing

suspended particles by creating currents (lateral cilia) and deflecting the padiway of particles onto the frontal surface

(latero-frontal cirri). vSiiitema & Jumars (1991) consider tiiat cilia diat are not protected from ambient flow may

be more important in manipulating and transporting captured particles ratJicr than in creating feeding currents.

Latero-frontal cirri could aid in retaining the particle-mucus complex onto the frontal surface during transport.

However, it is difficult to hypothesize and role lor die lateral cilia except for the creation of a feeding current.

These cilia are adjacent to the frontal surface (to assist to particle retention) and beat in metachronal waves creating

currents directed towards die frontal surface.

CONCLUSION

Spionid polychaetes have been and will continue to be important experimental species in applying optimal

foraging tiieory to marine and estuarine systems (Taghon, 1982; Taghon & Jumars, 1984) and in understanding

the role of near-bottom hydrodynamics in feeding behavior (Jumars, 1993). Spionid polychaetes are excellent

experimental subjects for feeding studies because (1) they feed at the sediment-water interface and are easily

observed, (2) many spionid species, especially estuarine species, are relatively hardy and survive well under

laboratory experimental conditions, and (3) most species place fecal rods at the surface which can be collected and

used to estimate feeding rates quantitatively under various experimental conditions. I Iowever, interpretation of data

and observations concerning feeding of spionids is complicated because (1) they have a mixed feeding mode

(deposit feeding, suspension feeding, bedload feeding) and (2) they posses a variety of morphological features that

may affect feeding behavior. Additional studies are necessary to clarify the roles of and possible interactions

between (1) functional ciliary groups, (2) mucus and (3) hydrodynamics in particle encounter, retention, transport

and rejection.

84

D M. DAUHR

Daro, M.N. & POLK. P., 1973. The autecology of Polydorci ciliata along the Belgian coast. Nelli. J. Sea Res., 6 :

130-140.

DaUER, D.M.. 1980. — Populations dynamics of the polychaetous annelids of an intertidal habitat in Upper Old Tampa

Bay, Florida. Ini. Rev. Ges. Hydrobioi. 65 : 461-487.

DaUER. D.M.. 1983. — Functional morphology and feeding behavior of Scolelepis squamata (Polychaela: Spionidae).

Mar. Biol., 11 : 279-285.

DaUER. D.M.. 1984. — Functional morphology and feeding behaviour of Streblospio benedicti (Polychaela; Spionidae).

In: P.A. HUTCHINGS (cd). Proceedings of the First International Polychaele Conference. Published by the Linnean

Society of New South Wales: 418-429.

DAUER, D.M.. 1985. — Functional morphology and feeding behavior of Paraprionospio pinnata (Polychaela:

Spionidae). Mar. Biol.. 85: 143-151.

DaUER. D.M.. 1987. Potential systematic significance of spionid polychaete tentacular morphology. Bull. biol. Soc.

Wash.. 1 : 4 1-45.

DaUER. D.M., 1991. Functional morphology and feeding behavior of Polydora commensalis (Polychaeta: Spionidae).

Ophelia Supplement 5 : 607-614.

DaUER. D.M. & Ewing, R.M.. 1991. — Functional morphology and feeding behavior of Malacoceros indicus

( Polychaeta : Spionidae). Bull. mar. Science, 48: 395-400.

DaUER. D.M.. MAYBURY, C.A. & EWING, R.M., 1981. — Feeding behavior and general ecology of several spionid

polychactcs from the Chesapeake Bay. J. Exp. Mar. Biol. Ecol., 54 : 21-38.

FaUCJIALD, K. & JUMARS.P.A.. 1979. — The diet of worms: a study of polychaete feeding guilds. Oceanogr. Mar. Biol.

Ann. Rev.. 17 : 193-284.

JORGENSEN. C.B.. 1981. — A hydromechanical principle for particle retention in Mytilus edulis and other ciliary

suspension feeders. Mar. Biol.. 61 : 277-282.

JORGENSEN. C.B., 1982. Fluid mechanics of the mussel gill: the lateral cilia. Mar. Biol.. 70 : 275-281.

JUMARS. P.A.. 1993. Concepts in biological oceanography. An interdisciplinary primer. Oxford University Press,

New York. 348 pp.

JUMARS, P.A.. SELF . R.F.L. & Nowell, A.R.M., 1982. — Mechanics of particle selection by lentaculate deposit-feeders.

J. Exp. Mar. Biol. Ecol.. 64 : 47-70.

Levin, L.A., 1981. — Dispersion, feeding behavior and competition in two spionid polychaetes. J. mar. Res., 39 : 99-

117.

LUCKENBACH, M.W., IlUGGETT . D.V. & Zobrist, E.C., 1988. Sediment transport, biotic modifications and selection

of grain size in a surface deposit-feeder. Estuaries. 11 : 134-139.

MORTENSEN. E. & Gai.TSOFF, P.. 1944. Behavior and tube building of Polydora ligni. Biol. Bull. (Woods Hole), 87 :

164-165.

SELF. R.F.L. & JUMARS. P.A., 1978. New resource axes for deposit feeders ? J. mar. Res., 36: 627-641.

Smimeta, J. & JUMARS. P.A.. 1991. Physical mechanisms and rates of particle capture by suspension feeders. Annual

Rev. Oceanogr. mar. Biol.. 29 : 191-257.

TAGHON, G.L.. 1982. — Optimal foraging by deposit-feeding invertebrates: roles of particle size and organic coating.

Oecologia, 52: 295-304.

Tagiion, G.L. & JUMARS, P.A., 1984. — Variable ingestion rate and its role in optimal foraging behavior of marine

deposit feeders. Ecology, 65 : 549-588.

Taghon, G.L.. Nowell, A.R.M. & Jumars.P.A.. 1980. — Induction of suspension feeding in spionid polychaetes by

high particle fluxes. Science, 210 : 562-564.

Wilson, H.IL. Jr. 1983. — The role of density dependence in a marine infaunal community. Ecology. 63 : 295-306.

Source .

9

Attributes of ribosomal DNA in alvinellid

polychaetes from hydrothermal vents

David R. DIXON * Linda R.J. DIXON * & Verena TUNNICLIFFE **

* Plymouth Marine Laboratory & Marine Biological Association

Citadel Hill

Plymouth PL1 2PB, UK

** School of Earth and Ocean Sciences

University of Victoria

B.C. Canada V8W 2Y2

ABSTRACT

The ribosomal DNA (rDNA) of three alvinellid polychaetes, Paralvinella palmiformis Desbruyeres & Laubier,

l\ pandorae Desbruyeres & Laubier and P. sulfmcola Desbruyeres & Laubier, from deep-sea hydrothermal vents in the eastern

Pacific Ocean, has been subjected to restriction-endonuclease digestion and the resulting restriction fragments compared with

those of Melinna palmata Grube, a member of a closely-related polychaete family, the Ampharclidae. An interesting feature of

the rDNA of representatives of both polychaete families was the tendency to cut with restriction enzymes containing an

increased number of G-C (guanine-cytosine) bases in their recognition sequences. Increased GC-content is known to confer

greater thermal and chemical resistance to the DNA molecule. This apparent similarity between the chemical composition of

rDNA of representative alvinellids and Melinna palmata , a shallow-water species which tolerates highly-reduced and metal-

rich sediments, suggests that this character may have arisen in the distant past primarily as an adaptation to chemically stressed

environments.

RESUME

Caractcristiques de PADN ribosomal de Polychetes Alvinellides des sources hydrothermales

Les ADN ribosomaux (ADNr) de trois polychetes alvinellides. Paralvinella palmiformis Desbruyeres & Laubier, P.

pandorae Desbruyeres & Laubier et P. sulfmcola Desbruyeres & Laubier. provenant des sources hydrothermales profondes de

lest pacifique. ont etc digeres par une endonuclease de restriction. Les fragments obtenus ont etc compares avec ceux de

Melinna palmata Grube. unc annelide polychete proche de la famille des alvinellides, les amphare tides. Un aspect important de

1’ADNr des polychetes cst leur tendance h se couper avec les enzymes de restriction contenant un nombre important de

sequence de bases G-C (Guanine-Cytosine) dans leurs segments de reconnaissance. L’augmentation de la sequence en G-C esi

connue pour conferer a l’ADN une plus grande resistance thermique et chimique. Cette apparente similarite enlre la

composition chimique de l’ADNr represen tatif des alvinellides et Melinna palmata, une espece d’eau peu profonde qui tolere

les sediments fortement reduils et charges en metaux, suggerent que ce caraclere a du se dcvclopper dans le passe comme une

adaptation au stress chimique de I'environnement.

Dixon. D.R., Dixon. L.R.J. & V. TUNNICLIFFE, 1994. Attributes of ribosomal DNA in alvinellid polychaetes from

hydrothermal vents. In: J.-C. Dauvin. L. KUJBIER & D.J. REISH (Eds). Actes de la 4eme Conference internationale des

Polychetes. Mdm. Mus. natn. Hist, not., 162 : 85-92. Paris ISBN 2-85653-214-4-165-2.

Source . MNHN. Paris

86

D.R. DIXON. L.R.J. DIXON & V. TUNNICLIFFE

INTRODUCTION

The polychaete family Alvinellidae is known only from hydrothermal vents in the Pacific Ocean

(DesbruyFres & LAUBIER, 1991). Two genera are described : Alvinella widi two species and Paralvinella with

nine species at vent sites on both sides of the Pacific. Alvinella species inhabit the sides of smokers on die East

Pacific Rise only and Uicy have substantial morphological alteration such as die insertion of bacterial filaments on

the dorsum. The smoker habitat on Juan de Fuca Ridge and Marianas back-arc basin is occupied by Paralvinella

sulfincola Desbruyfcres & Laubier and Paralvinella hessleri Desbruy£res & Laubier, respectively. Odier

paralvinellid species live among vestimentiferan tubes or in sediments where the potential for high temperature

encounters is low.

The alvinellid family has several characteristics reminiscent of die hypotheucal ancestor of die terebellomorph

order. The current model of systematic relationships among die alvinellid species is based on morphological

analyses (DESBRUYfcRES & Laubier, 1991). Alvinella is the most derived genus. Widiin Paralvinella , there are

four distinct morphological subgroups: P. pandorae is die most distinct and nearest the ancestral form while P.

palmiformis and P. sulfincola belong to one subgroup marked by die form of the buccal tentacles. Although die

latter two species share many features and are often collected togedier, genetic distance based on allozymes

clearly differendates the species (Tunnicliffe et al., in press).

This study examines three species from the Juan de Fuca Ridge: Paralvinella pandorae pandorae Desbruyfcres

& Laubier, P. palmiformis Desbruybres & Laubier and P. sulfincola Desbruyfcres & Laubier. Habitat observadons

suggest that there is a preference for habitats widi vent temperatures increasing in die order listed (Fig. 1). P. p.

pandorae builds mucous sheaths in vestimentiferan clumps while P. palmiformis is sedentary but free-ranging in

these lower temperature clumps and on sulphide chimneys formed by high temperature fluids (TUNNICLIFFE et al.,

1985; DESBRUYkRES & Laubier, 1986). P. sulfincola is only found on sulphide chimneys and, in the greatest

numbers, widiin centimetres of superheated fluids (Tunnicliffe et al. , in press). Observations of die proximity of

certain species to fluid flows in excess of 100 °C challenge current dogma that molecular stabilisation in

metazoans requires temperatures less than 60 °C (Brock, 1985).

+A . pompejana +

+-A . c a u d a t a ►

< — P. sulfincola — h

P . hessleri

Fig. 1. Approximate habitat ranges of alvinellid species. Hotter temperatures may range up to 65 °C as turbulent mixing

carries blasts of hot water over the worms. There are no long-term records of chimney habitat temperatures to document

actual ranges. Spot measurements and observations are the bases for this diagram. Little information is available for P.

hessleri.

P . palmiformis —+

P . g r a s s I e / — ►

P. pandorae

We recently reported die results of experiments which showed diermal stability of rDNA from a range of

hydrothermal vent species (largely alvinellid polychaetes) was positively correlated widi environmental

temperature (Dixon et al, 1992). This was attributed to a supposed increase in G-C (guanine-cytosine) content of

the rDNA molecule. Increased G-C content confers increased thermal and chemical stability to the DNA molecule

which is dependent on the number of hydrogen bonds: A-T (adenine-thymine) base pairs are linked by two bonds

rDNA IN HYDROTHERMAL VENTS POLYCIIAETES

87

whereas G-C pairs arc linked by three (e.g. DARNELL et aL 1986). This paper presents further evidence, based on

restriction analysis results, of increased G-C levels in the rDNA of hydrothermal vent polychaetes and a dose

relative from highly-reduced and metal-rich, shallow-water environments, which suggests this character may have

arisen in the distant past primarily as an adaptation to hostile chemical conditions.

FIG. 2. Hybridisation analysis of genomic DNA from a single Paralvinella palmifonnis. (A) Photograph of 1% agarose gel

after running at 30 volts for 16 h (0.1 volts cm’1 h1) and ethidium -bromide staining, showing numerous satellite bands.

(B) After Southern transfer and hybridisation with the 2.9 kb pVW-PCR ( P . palmifonnis rDNA-) digoxygenin-labelled

probe. Lanes 1 and 14. Lambda-Hindlll DNA molecular-weight marker; Lane 2, Sail-digested Mytilus edulis genomic

DNA (control) showing a characteristic 3.6 kb fragment; Lane 3. DNA molecular weight marker, pBR328 cleaved with

Bgll and Hinfl; Lanes 4-13 , P. palmifonnis genomic DNA: Lane 4, EcoRI/HindBI double digest; Lane 5. BamHI/EcoRI

double digest; Lane 6, Sall/Hindlll double digest; Lane 7. Sall/BamHI double digest. Note, suspected partial; Lane 8,

undigested DNA; Lane 9, Sall/EcoRI double digest; Lane 10, Hindlll digest showing absence of cutting sites within the

repeat unit (cf. also lanes 6 and 13); Lane 11, EcoRI-digest; Lane 12, BamHI-digest; and Lane 13, Sail -digest.

D.R. DIXON. L.R.J. DIXON & V. TUNNICLIFFE

MATERIALS AND METHODS

Specimen collection

The three paralvinellid species were collected by submersibles on Juan de Fuca Ridge at two sites 100 kin

apart. Ten P. palmiformis specimens came from two vents on Axial Seamount (44°58.9' N, 130° 13.3' W)

and one vent on Cleft Segment (44°57.4'N, 130°I3.8'W). The three P. p. pandorae specimens came from one vent

at each site and P. sulfincola , two specimens, came from the base of a smoker at 44°58.9* N, 130° 13.3' W. Another

terebellomorph polychaete, the ampharetid M. palmata and the serpulid Pomatoceros lamarckii were collected

subtidally at Plymouth, England: the dog-whelk Nucella lapillus and the mussel Mytilus edulis came from

intertidal populations in southeast Cornwall.

Tissue handling andDNA extraction

High-molecular-weight DNA was purified by overnight digestion with proteinase K followed by repeated

phenol/chloroform extractions. All DNA samples were treated with RNAse (SAMBROOK et at., 1989). After

ethanol precipitation, DNA was vacuum dried and dissolved overnight in TE (10 mM Tris, 1 mM EDTA, pH 8.0),

and stored at 4°C for short periods or frozen at -20°C. Degraded DNA samples, identified by smearing on gels,

were not included in the analysis.

Restriction analysis

Thirteen 6-cutter restriction endonucleases (Boehringer-Mannheim) were used singly and in combination on

replicate samples of DNA : BamHI, Dra, EcoRI, EcoRV, Hindlll, Kpnl, PstI, PvuII, SacI, Sail, Smal, Xbal and

Xhol.

Approximately 2.5 mg of DNA was cut with restriction endonucleases according to the manufacturer's

instructions. The DNA fragments were sorted according to size by gel electrophoresis using a 1 % agarose gel in

TBE buffer (90 mM Tris-HCL, 0.89 mM boric acid, 2.5 mM EDTA, pH 8.3). Running conditions were 33 volts

for 22 hours at room temperature. Gels were stained with cthidium bromide, photographed using IJV-light, and llie

DNA blotted onto a nylon membrane (Genescreen, Dupont) (Southern, 1975).

rDNA probes

Homologous probes were manufactured by polymerase chain reaction (PCR), using PCR primers flanking

regions 5 to the 18S and 28S genes (e.g. HOLLAND et al. , 1991), and cloned by conventional bacterial methods. A

heterologous probe representing the entire rDNA repeat unit (pCtp 1550), (Schmidt et al., 1982) was used alter it

had first been digested with Hindlll and EcoRI to improve the labelling and hybridisation efficiencies. A non-

radioactive DNA labelling and detection procedure was employed in this study (digoxygenin, KESSLER et al.,

1990).

RESULTS

Restriction analysis

Figure 2 shows digestions of P. palmiformis rDNA with a range of restriction endonucleases, singly and in

combination. Figure 2A is a representative agarose gel stained with ethidium bromide and photographed under

IJV-light to reveal numerous satellite bands. Fig. 2B shows die same panel of DNA when transfered to a nylon

filter and labelled widi a 2.9 kb VW- PCR probe (based on P. palmiformis, 5' 18S - 5' 28S rDNA region). The

DNA fragments revealed by the probe(s) were used to map the rDNA repeal unit.

Table I shows die enzyme cutting results for diree coastal and two hydrothermal-vent species. The probe used

was pCtp 1550 (Schmidt et al., 1982) which has die potential to span the entire length of die repeat unit. Repeat

unit lengdi was estimated for the different species based on die combined lengths of die fragments produced by

Sail digestion. In die case of M. palmata, which lacks a Sail in its repeat unit, the size was estimated from the

combined fragment sizes produced by separate BamHI. EcoRI, SacI and PstI digests. M. edulis DNA was

the only one which cut with all 13 enzymes. With the exception of M. palmata . die number of enzymes which cut

was inversely related to die size of die repeat unit. This relationship held when die comparison was made based on

the size of the large non- transcribed spacer (NTS), indicating that die number of enzymes cutting was not simply

a function of sequence lengdi. Based on the number of G and C bases in the recognition sequences of die enzymes

Source

rDNA IN HYDROTHERMAL VENTS POLYCHAETES

89

which cul within the rDNA, the rDNA of the two hydrothermal vent polychaetes appears GC-rich, i.e. has a

higher G-C index, compared to the three shallow-water species ('Fable 1).

TABLE 1.— Recognition sequences of restriction endonucleases. G-C indices (on a scale of 0 - 6), and individual species

scores: Paralvinella palmiformis, (P. palm. ); P.p .pandorae. (P. pand. ); Melinna palmata, (M. palm. ); Nucella lapillus

(N. lap.); and Mytilus edulis. (A/, edulis).

Paralvinella palmiformis

XS ESm

-TZ -?J.

Sa

-*T

B Sm

▼ ▼

Sm Sa Sm

T T ▼

Sa E

▼ T

- T

P

A"

D

Paralvinella pandorae

xs E

zz z

18S 5.8S 28S

DPS

▼ ▼

3-tH

Sm

B

▼

P Sa

▼ ▼

ITS-1 ITS-2

- 1k.

NTS

1 kb

PIG. 3. — Restriction map of rDNA repeat unit of Paralvinella palmiformis and P. pandorae. Polymorphic restriction sites in

P. palmiformis arc indicated by open triangles. Restriction endonucleases which showed completely different cleavage

patterns in the two species are shown below the restriction map of P. palmiformis. ITS-1 and ITS-2 = internal transcribed

spacers; NTS = large non -transcribed spacer region; and 18S. 5.8S and 28S = the three rRNA-genes coding for the

ribosomal subunits. B = BamHI; D = Dral; E = EcoRI; H = MindHI; P = PvuII; S = Sail; Sa = SacI; Sm = Smal; and X =

Xhol. The estimated 1.5 kb difference in repeat unit size was attributed to inter- specific variation in the size of the NTS

region, indicated by the shaded portion in the map of P. pandorae. However, no enzyme was discovered which mapped to

this region so confirmation must await the results of further investigations.

Source :

90

D R. DIXON, L.R.J. DIXON & V. TUNNICLIFFF.

The diree species of Paralvinella which were analysed for their rDNA slruciure had repeat unit lengths in the

range 11 - 12.5 kb. This was significantly larger than die 7.2 - 7.6 kb values found for the three shallow-water

species (one polychaete, two molluscs). The difference in repeat unit length between P. pandorae and

P. palmiformis was traced to a duplication or some other sequence insertion affecting die NTS (Fig. 3). The

significant differencein repeat unit lengdt between Melinna palmata (7.5 kb) (Family Ampharetidae) and these

diree paralvinellids agrees with the conventional taxonomic separation of diese two polychaete families.

Restriction mapping

Restriction sites for a total of eight enzymes were mapped for P. palmiformis and nine enzymes for P. p.

pandorae-, the extra one being HindNI (Fig. 3). These two species shared 10 restriction sites in common (37 %)

out of a total of 27 mapped (Fig. 4). In contrast, P. sulfincola shared only four sites (22 %) in common with P.

palmiformis , out of a total of 18 identified (Dixon & DIXON, unpublished), which may indicate a closer

relationship between die former two species. (Note: insufficient high-quality DNA was extracted from the few

specimens of P. sulfincola to carry out any detailed mapping of restriction sites.) Allowing for some heterogeneity

between repeats and a degree of inter-individual restriction-site polymorphism, diese data suggest that P.

palmiformis is more closely related to P. p. pandorae than cither is to P. sulfincola. Clearly, molecular adaptation

to high temperature will have played an important part in speciation widiin this group. By way of contrast, the

ampharetid Melinna palmata shared only six enzymes in common with the two paralvinellids (Table 1), and

differed greatly in the number and size of fragments which diese generated. The bulk of die variation in cleavage

sites between P. palmiformis and P. p. pandorae mapped to genic regions widiin die rDNA repeat unit, although

several polymorphisms were traced to the non-coding NTS. Lacking sequence information it is not possible to

distinguish between introns and exons widiin genes. It seems highly probable that at least some of diis inua-genic

variation will involve "silent sequences", i.e. non-coding sequences which typically evolve rapidly (Li et al.,

1985).

DISCUSSION

Recently, we reported die results of experiments designed to investigate die relationship between thermal stability

of DNA and the physical and chemical conditions experienced by hydrothermal vent organisms (DIXON et al„

Paralvinella pandorae

Paralvinella palmiformis

Paralvinella sulfincola

0 10 20 30 40 50 60 70 80 90 100

I _ | _ I _ 1 _ I _ _L - 1 - 1 - 1 - 1 - 1

Percentage difference

FlG. 4. — Unrooted tree based on percentage restriction-site differences between three species of Paralvinella from the Juan

de Fuca Ridge.

rDNA IN HYDROTHERMAL VENTS POLYCHAETES

91

1992). A positive correlation was round between the denaturing temperature of rDNA and environmental

temperature for seven alvinellid species which was thought to be due to an increase in GC-content. In other

organisms, increased GC-content has been shown to confer greater thermal and chemical stability to the DNA

molecule (Darnell et al. , 1986), and is an interesting molecular adaptation to hostile environmental conditions

(e.g. BERNARDI & BERNARDI, 1990a, b). The results of the present investigation provide further evidence of

increased GC-levels in the rDNA of some hydrothermal vent polychaetes and a shallow-water ampharetid, M.

polmata (Table 1). The family Alvinellidae is closely related to, and perhaps derived from, the ampharetid

polychaetes (Desbruy6res & Laubier, 1986). The evidence presented here for increased GC-content in M.

palmcita , which tolerates highly-reduced and metal-rich sediments (Gibbs et al. , 1981), indicates that what may

have arisen originally as an adaptation to harsh chemical conditions in shallow-water sediments, may have

permitted colonisation of the high-temperature, and chemically hostile, hydrothermal vent environment in die

distant past by a common ancestor (TUNNICLIFFE, 1992).

The topology of the unrooted tree shown in Figure 4 is divergent from present systematic relationships based

on morphology which places P. p. pandorae as the most ancestral species of the genus. All other paraJvinellid

species have a different branchial form; among these species P. palmiformis and P. sulfincola form a sub-group

with trifoliate tips on the buccal tentacles (DESBRUYfeRES & Laubier, 1991; TUNNICLIFFE et al ., 1993). A study

of allozyme similarity among these species confirms the distance of P. p. pandorae but also makes a strong

differentiation between P. sulfincola and P. palmiformis (D. Jollivet, pers. comm.). That morphological and

molecular interpretations differ may be a function of the strong selection that is likely present on molecular

functioning in an extreme habitat; morphological response may not be so strong. However, phylogenetic

comparison of sequences that differ by more than 25 % is not recommended (Upholt, 1977); with greater

differences there is increased probability that cleavage sites may be convergent (Dowling et al. , 1990). The

apparently high degree of divergence of these three species (up to 60 %) may reflect long evolutionary time,

strong selection pressures, or both. While no certain fossil record is available, there are Cretaceous vent deposits

with tubes reminiscent of those of Alvinella species (Haymon & Koski, 1985); a large proportion of the vent

fauna may be a Mesozoic relic (TUNNICLIFFE, 1992). High copy number sequences are generally not good

candidates for constructing phylogenetic trees (HiLLlS & Moritz, 1990) and further work is required before good

systematic relationships can be established among these species.

ACKNOWLEDGEMENTS

The bulk of this work was funded by the UK Natural Environment Research Council through a rersearch grant

to Prof. A.J. Southward; VT was funded by NSERC Canada. Dr Peter Holland (Oxford University) kindly

donated several of the rDNA probes. We are grateful to David NICHOLSON for photographic assistance.

REFERENCES

BERNARDI, G. & BERNARDI G.. 1990a. — Compositional transitions in the nuclear genomes of cold-blooded vertebrates. J.

mol. Evol. , 3 1 : 282-293.

Bernardi. G. & BERNARDI G.. 1990b. — Compositional patterns in the nuclear genomes of cold-blooded vertebrates. J. mol.

Evol. ,31 : 265-281.

Brock, T.D., 1985. — Life at high temperatures. Science , 230 : 132-138.

DARNELL. J., LODISH, H. & Baltimore. D.. 1986. — Molecular Cell Biology. Scientific American Books. New York. 1 192

pp.

DesbruyEres, D. & Laubier, L., 1986. — Les Alvinellidae. une famillc nouvellc d'annelides polychetcs infcodccs aux

sources hydrothermales sous-marincs : systematique, biologic etecologie. Can. J. Zool. , 64 : 2227-2245.

DesbruyLres, D. & Laubier, L., 1991. Systematics, phylogeny. ecology and distribution of Alvinellidae (Polychaeta)

from deep-sea hydrothermal vents. Ophelia SuppL. 5 : 31-45.

DIXON, D.R.. Simpson- White. R. & Dixon. L.R.J.. 1992. — Evidence for thermal stability of ribosomal DNA sequences in

hydrothermal -vent organisms. J. mar. biol. Ass. J.K.. 72 : 519-527.

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DOWLING, T.E.. MORITZ. C. & PALMER, J.D.. 1990. Restriction site analysis. In: D.M. HlLLIS & C MORITZ (eds).

Molecular Systematics. Sinauer Associates Inc.. Sunderland. Mass. : 250- 317.

GIBBS. P.E., BRYAN. G.W. & Ryan. K.P.. 1981. — Copper accumulation by the polychaete Melinna palmata: an antipredation

mechanism? J. mar. biol. Ass. U.K. . 61 : 707 - 722.

IlAYMON, R.M. & KOSKI. R.A.. 1985. — Evidence of an ancient hydrothermal vent community: fossil worm lubes in

Crelaceaous sulfide deposit of the Samail Ophiolite. Oman. Dull. Biol. Soc. Wash., 6 : 57-65.

HlLLIS. D.M. & Moritz. C.. 1990. Molecular Systematics. Sinauer Associates Inc.. Sunderland. Mass., 588 pp.

HOLLAND, P.W.H.. Hacker, A.M. & Williams. N.A., 1991. — A molecular analysis of the phylogenetic affinities of

Saccoglossus cambrensis Brambell & Cole (Hemichordata). Phil. Trans. R. Soc. Loud. B., 332 : 185-189.

KESSLER, C.. Holtke, H.J.. Seibl. R.. Burg, J. & Muhlegger. K.. 1990. — Non-radioactive labelling and detection of

nucleic acids: I. A novel DNA labelling and detection system based on digoxygenin: anli-digoxygenin ELISA principle.

Biol. Chem. Hoppe Seyler, 371 : 917-927

Li. W.-H., Wu, C.-I. & LUO, C.-C., 1985. A new method for estimating synonymous and nonsynonymous rates of

nucleotide substitution considering the relative liklihood of nucleotide and codon changes. Mol. Biol. Evol. , 2 : 150- 174.

Sambrook. J .. FRITSCH. E.F. & Maniatis. T., 1989. -- Molecular cloning. A laboratory manual , vol. 1. 2nd edition. Cold

Spring Harbour Laboratory Press.

SCHMIDT, E.R., Godwin. E. A., KEY!., II. -G. & Israelewski, N.. 1982. — Cloning and analysis of ribosomal DNA of

Chironomus thummi piger and Chironomus thummi thummi. Chromosoma (Berlin). 87 : 389-407.

South KILN. E.. 1975. - Gel electrophoresis of restriction fragments. Meth. Eniymol., 68 : 152-176.

TUNNICLIFFE. V., 1992. The nature and origin of the modern hydrothermal vent fauna. Palaios, 7 : 338-350.

TUNNICLIFFE, V.. JUNIPER. S.K. & do BURGH, M.E.. 1985. The hydrothermal vent community of Axial Seamount, Juan dc

Fuca Ridge. Biol. Soc. Wash. Bull.. 6 : 453-464.

TUNNICLIFFE, V.. DESBRUYERES, D.. Jollivet, D. & Laubier, L.. 1993. Systematic and ecological characteristics of

ParalvineUa sulfincola Desbruyeres and Laubier. a new polychaete (family Alvinellidae) from Northeast Pacific

hydrothermal vents. Can. J. Zool., 71 : 286-297.

UPHOLT, W.B., 1977. — Estimation of DNA sequence divergence from comparison of restriction endonuclease digests. Nucl.

Acids. Res.. 4 : 1257-1265.

Source :

10

On the nature of the two anterior asetigerous rings

in Dorvilleidae and Dinophilidae

(Annelida, Polychaeta)

Danny EIB YE-JA COB SEN

Zoological Museum

Univcrsitetsparken 15

DK-2100 Copenhagen 0

Denmark

ABSTRACT

Members of the order Eunicida are apparently characteristic in possessing two more or less clearly separated rings between

the prostomium and the first setigcr. In the family Eunicidae it has previously been shown that these rings represent a

subdivision of the peristomium related to the manner in which the longitudinal muscles are attached to the body wall.

Nevertheless, this character may be a synapomorphy for Eunicida. provided that it is homologous among it s members. This

hypothesis is tested in members of the families Dorvilleidae and Dinophilidae through light microscopic studies of the body

area in question. Recent publications have proposed that Dinophilidae is closely related to or actually a subtaxon of

Dorvilleidae; this conclusion is not contradicted by the results of this investigation.

RESUME

Sur la nature des deux anneaux asetigeres anterieurs reunis chez les Dorvilleidae et les Dinophilidae (Annelida

Polychaeta)

Les membres de 1'ordre Eunicida paraissent caracterises par la possession de deux anneaux plus ou moins nettement

separcs entre le lobe cephaliquc et le premier setigere. Pour la famille des Eunicidae on a demontre que ces anneaux

repre sen tent des subdivisions du peristomium en relation avec la manicre par laquclle les muscles longitudinaux sont attaches

aux parois du corps. Neanmoins, ce caractere peut ctre une synapomorphie pour les Eunicida, a condition qu’il soit homologue

parmi ses membres. Cette hypothese est mise a I'epreuve chez les membres des families des Dorvilleidae et des Dinophilidae

par des etudes microscopiques de cette region du corps. Dans des publications recentes, on a propose que les Dinophilidae sont

effectivement ctroitement allies a un sous-taxon des Dorvilleidae; cette conclusion n'est pas en contradiction avec les resultats

de cette investigation.

INTRODUCTION

In most members of the polychaete family Dorvilleidae the peristomium takes the form of two apodous rings

between die prostomium and die first setiger. In most species diese rings are subequal, but in many die anterior

ElB YE- JACOBSEN, D., 1994. On the nature of the two anterior asetigerous rings in Dorvilleidae and Dinophilidae

(Annelida, Polychaeta). In: J.-C. Dauvin. L. Laubier et D.J. REISH (Eds), Actes de la 4eme Conference internationale des

Polychetes. Mem. Mus. natn. Hist. nat.. 162 : 93-100. Paris ISBN 2-85653-214-4.

Source : MNHN. Paris

94

D. EIBYE-JACOBSEN

one is shorter and indistinctly separated from the prostomium. Only few species show no trace of peristomial

subdivision, e.g., four of die five hitherto described species of the genus Exallopus Jumars, 1974 (die exception is

die type species, E. cropion Jumars. 1974). Some confusion has surrounded die nature of diese two rings. Thus,

while many audiors have preferred neutral terms, such as rings, others appear to have regarded them as true

segments (e.g.. Jirkov, 1989). where Dorvilleidae is characterized as having "two peristomial segments without

parapodia, setae or cirri". The use of die word "segment" may in many instances have been coincidental, but in an

evaluation of dorvilleid relationships widi other polychaete groups it is important to understand the true nature of

these rings. Within the order Eunicida conditions similar to (hose in Dorvilleidae are found in Eunicidac,

Lumbrineridae (sensu ORENSANZ, 1990. including Lysaretidae), Hartmaniellidae. Oenonidae (= Arabellidae), and

Iphitimidae (members of the families Histriobdellidae and Ichdiyotomidae are too strongly modified to allow an

assessment of this character). The major group in which only one peristomial ring is present is the family

Onuphidae, which is considered die sister group of Eunicidac (ORENSANZ, 1990; FaUCHALD. 1992). Descriptions

of die larval development of onuphids are not clear as to whether a peristomial subdivision is present during

earlier stages in ontogeny (e.g.. Hsieh & Simon 1987 on Kinbergonupliis simoni). In his discussion of larval

development in Nothria elegans, Blake (1975a) refers to die presence of such a subdivision but this is not

confirmed by his illustrations.

The term peristomium, as it is currently used, is not applied to homologous structures in various polychaete

families. In embryological terms, the peristomium has its origin in the region between the prototroch and the

telotroch of the classical trochophora larva (e.g.. George & Hartmann-Schrodf.r, 1985). This appears to be die

case in Eunicida (see below). However, die adult peristomium of many polychaete families is a compound

structure consisting of the peristomium s. sir. as well as a variable number of anterior segments of teloblastic

origin which have often lost their setae and parapodia and may possess paired tentacular cirri. Examples of these

conditions may be seen in families such as Hesionidae, Syllidae, and Nereidae (Gilpin-Brown, 1958).

For Eunice kobiensis (Eunicidae), Akesson (1967a) gave a very convincing account of the embryological

origin of the peristomium. According to his studies, die first setiger of adults corresponds to the first larval

segment; the peristomium, including both rings and the peristomial cirri, must be intcipreted as presegmentai.

Akesson also provided an anatomical explanation for die strongly developed peristomial subdivision, which is

found in this species. His studies showed that in die posterior region of (he peristomium a number of fibres

belonging to the ventral longitudinal muscle bands branch off in a lateral direction and attach themselves to die

body wall at die level of the subdivision (Akesson, 1967a: Fig. 1 1). In a similar manner, fibres of die dorsal

longitudinal muscles give rise to die dorsal component of die visible, non-segmental furrow.

Assuming that the absence of any peristomial subdivision in Onuphidae may be regarded as a secondary

phenomenon (possibly related to dieir being mostly tubicolous). the presence of two rings of true peristomial

origin may be regarded as an autapomorphic character of Eunicida. Embryological observations indicate diat

Akesson's observations on Eunice are valid for members of Dorvilleidae (e.g., Akesson, 1967b, 1973a, and b on

various species of Ophryotroclw, Blake, 1975b on Dorvillea rudolphi) in die sense that the two asetigerous rings

are of peristomial origin. However, it remains to be demonstrated dial a true homology exists, i.e., that a

homologous pattern of muscle attachment is present.

The primary purpose of this paper is to examine whether anatomical observations on various species of

Dorvilleidae can confirm a homology on diis point.

The family Dinophilidae was previously placed in Archiannelida, which was usually accorded order or class

rank. In recent years, a body of evidence has grown diat points to a close relationship between this family and

Dorvilleidae (Akesson, 1977; Westheide, 1985. 1987; Orensanz, 1990; Eibye-Jacobsen & Kristensen, in

press). However, since dinophilids are greatly reduced and highly specialized, much of die evidence is

FIG. I . A-C. Protodorvillea kefersteini, sagittal section showing ventrolateral longitudinal muscle band and attachment of

accessory peristomial fibres to body wall at mid-peristomial furrow (A); cross section showing accessory peristomial fibres

(in close proximity to ventrolateral longitudinal muscle band) attached to body wall (B); cross section 15-20 mm further

posterior through anterior margin of mandible showing as yet undivided, strongly developed ventrolateral longitudinal

muscle band (anterolateral, accessory mandibular teeth visible on left side) (C). D. Ophryotrocha cf. harlmcmni, cross

section, on right side corresponding to B (pharynx protruded). All scales = 10 mm. Nomarski differential interference

contrast used on all figures. Abbreviations: al = aciculum of first setiger; a2 = aciculum of second setiger; a3 = aciculum

of third setiger: amt = accessory mandibular teeth; ant = anterior peristomial ring (first post-prostomial ring); apf =

accessory peristomial fibres; cc = circumcsophagcal connective; m = mandible; mpf = mid-peristomial furrow; ol =

oesophageal lumen; pb = pharyngeal bulbus; pi = pharyngeal lumen; pos = posterior peristomial ring (second post-

prostomial ring); vc = ventral ciliation; vim = ventrolateral muscle band; vne = ventral nerve cord.

ANTERIOR ASETIGEROUS RINGS IN DORVILLEIDS AND DINOPHIUDS

95

Source : MNHN , Paris

96

D. ED3YE-JAC0BSEN

circumsiantial (larval resemblances, connections through theoretical morphological reduction series, parasite

relationships; see above references for discussion). It has been difficult to find positive apomorphic characters that

support a relationship. To date, the best such indication is the presence of an unpaired, pygidial stylus with a

specific musculature in certain dorvilleid genera and most members of the dinophilid genus Dinophilus

(WESTHE1DE, 1985).

There arc difficulties in the homologisation of segments in dinophilids with those of odier polychaetes, since

parapodia and setae are absent. However, a peri&tomial subdivision resembling that in Dorvilleidae appears to be

present, most clearly in the genus Trilobodrilus . The present study was in part undertaken to isolate yet another

possible character to strengthen the view of a close relationship between these families (or at least, in the present

context, the membership of Dinophilidae in Eunicida).

MATERIALS AND METHODS

Several specimens of each of the following species were examined: Protodorvillea kefersteini (McIntosh,

1869); Parougia eliasoni (Oug, 1978); Ophryotrocha cf. hartmanni Huth, 1933: 0. puerilis siberli (McIntosh,

1885): and Trilobodrilus cf. nipponicus Uchida & Okuda. 1943. The dorvilleid species were taken at various

localities along the north coast of Brittany, France. The specimens of Trilobodrilus were found in samples of

coarse sand and gravel taken off Ellekilde Mage in the southern Kattegat, Denmark.

The specimens were embedded in paraplast using standard techniques, sectioned to a thickness of 4 mm, and

stained using a modification of Masson's trichrome method (Weigcrt's iron haemotoxylin. Ponceau's xylidinc, and

Fast Green). This renders muscle tissue bright red, whereas collagen and other connective structures arc stained

green. After dehydration, die sections were embedded in Entellan.

The sections were studied with a Leitz Ortholux microscope, whereas photographs were taken on a Zeiss

Axiophot microscope, in most cases employing Nomarski differential interference contrast.

RESULTS

Protodorvi Ilea keferstei n i

In the posterior part of die second asetigerous ring a group of muscle fibres (henceforth termed accessory

peristomial fibres) leave die lateral part of each ventrolateral longitudinal muscle trunk (Fig. 1C). They attach to

the body wall ventrolaterally on eidier side, midway along die length of the peristomium (Fig. IB). Figure 1A

shows a sagittal section in which a ventrolateral longitudinal muscle band is seen in the anterior setigers as well as

the attachment of die accessory peristomial fibres to the body wall at the mid-peristomial furrow.

The ventrolateral longitudinal muscle trunks continue forward and insert on the body wall at the lower

(posterior) lip of the mouth opening (not visible on Fig. 1A). These fibres may be confused widi those of die

anterior mandibular protractor muscles, which are also attached to the lower lip (Dales, 1962; not shown on

Akesson's (1967a) figures). However, the latter are inserted in a midventral position, whereas die paired

ventrolateral longitudinal muscle trunks are ventrolaterally attached.

Accessory peristomial fibres also branch off from the dorsolateral longitudinal muscle trunks and are attached

to the body wall furdier forward at the level of peristomial subdivision.

Parougia eliasoni

Observations on diis species were identical to diose described for Protodorvillea kefersteini.

FIG. 2. — Trilobodrilus cf. nipponicus. cross sections showing body becoming increasingly narrow in anterior portion of

second post-prostomial ring, at narrowest point (D) showing subdivision of ventrolateral longitudinal muscle bundle, the

dorsal component of which may be homologous to accessory peristomial fibres in Dorvilleidae. Scale A-D = 10 mm.

Nomarski differential interference contrast used on A-C. Abbreviations: al = aciculum of first seliger; a2 = aciculum of

second setiger: a3 = aciculum of third setiger; amt; = accessory mandibular teeth: ant = anterior peristomial ring (first post-

prostomial ring); apf = accessory peristomial fibres; cc = circumesophageal connective; m = mandible; mpf = mid-

peristomial furrow; ol = oesophageal lumen; pb = pharyngeal bulbus; pi = pharyngeal lumen; pos = posterior peristomial

ring (second post-prostomial ring); vc = ventral ciliation; vim = ventrolateral muscle band; vne = ventral nerve cord.

Source

ANTERIOR ASETIGKROUS RINGS IN DORVILLEIDS AND DINOPHIL.IDS

97

Source ; MNHN , Paris

98

D. EIBYE-JACOBSEN

Ophryotrocha cf. hartmanni

The sectioned material of this species, although of a poorer quality, shows the presence of accessory

peris tomiaJ fibres (Fig. ID) attaching to the bexly wall at die level of the mid-peristomial furrow. As in the other

dorvilleids that were examined, the accessory fibres branch off from die ventrolateral muscle bands in die

posterior part of die second peristomial ring. The animal shown was fixed with the pharynx somewhat protruded:

die accessory peristomial fibres are contracted and therefore the two posterior mandibular rods ;ire visible. It was

not possible to observe whether dorsal accessory fibres are present.

Ophryotrocha puerilis siberti

Observations on diis species were as described for 0. cf. hartmanni.

Trilobodrilus cf. nipponicus

From the middle of die second post-prostomial ring (Fig. 2A) to die furrow between the first and second rings

(Fig. 2D) body width decreases from 54 mm to 38 mm. Observations on the possible presence of accessory

peristomial fibres was hampered by the small size of the animals in question. Thus, in any given cross section each

ventrolateral muscle band consists of 2-4 cells only. However, at die level of die furrow between die first two post-

prostomial rings, die dorsalmost of these cells appears separated from the others. It was not possible to observe

whether it was attached to die body wall at this point, but this cell is absent on more anterior sections, indicating

that its rostral end must be very close to the furrow.

DISCUSSION

In die dorvilleid species studied, subdivision of the peristomium appears to be induced (at least in part) by the

attachment of accessory muscle fibres with an origin in the longitudinal trunks. These observations correspond to

diose reported by Akesson (1967a) for Eunice kobiensis . die only important difference being that die accessory

fibres remain close to the main trunk throughout their entire length. In Eunice (as indicated on Akesson's

drawing) the ventral accessory peristormial fibres and the ventrolateral muscle bands appear to be clearly

separated rostrally. This disparity may be due to differences in degree of muscle contraction.

Recently, Orensanz (1990) has suggested that a number of dorvilleid genera, among diem Ophryotrocha

should be placed in the family Iphitimidae. Doubtless a close relationship between Dorvilleidae and Iphiumidae

exists. However, as the character studied in the present paper is most likely common to die entire order Eunicida, it

probably has no bearing on inter-familial relationships. The question of whether Orensanz* rearrangement of

genera is justified will be treated in a separate paper (Eibye-Jacobsen & KRISTENSEN, in press).

The accessory peristomial fibres and thus the subdivision of die peristomium in Dorvilleidae are very probably

homologous to those in Eunicidae. Although corresponding anatomical studies have not yet been carried out on

members of families such as Eumbrineridae and Oenonidae, and disregarding the aberrant conditions in

Onuphidae, the presence of a secondary peristomial subdivision in association with a specific pattern of muscle

attachment appears to be an autapomorphic character for die order Eunicida. Even though external signs of

genuine peristomial subdivision are lacking in odier polychaete groups, ii would be preferable to lest this

hypodicsis by carrying out corresponding studies on some of them. The sister group of Eunicida would be of

special interest. Unfortunately, it is at the present time difficult to form an informed opinion as to which

polychaete groups are likely candidates, as Eunicida is generally considered a somewhat isolated group (Dales,

1962; Storch, 1968; Fauchald, 1977).

On die basis of the present study of Trilobodrilus , it is neither possible to conclude that accessory peristomial

fibre(s) exist nor diat the two anterior post-prostomial rings represent a subdivided peristomium. The results are

too uncertain and die apparent presence of a muscle cell disassociated from the others of the ventrolateral

longitudinal muscle band (Fig. 2D) may be due to an artifact. The fact that this cell has a dorsolateral position

relative to die longitudinal muscle band (lateral in Dorvilleidae, ventrolateral in Eunicidae) should not be seen as a

hindrance to considering die phenomenon (if it exists) as homologous. In all cases, the fibres that branch off are

the most lateral ones and it is the orientadon of the longitudinal muscle bands which varies. Ultrastructural studies

must, however, be carried out before it can confidently be concluded diat a homology does exist on this point

between dinophilids and eunicidans.

Akesson (1967a) and subsequently other audiors have suggested diat the funedon of die accessory peristomial

fibres is to augment the operation of the complicated jaw apparatus present in members of the order Eunicida. No

Source :

ANTERIOR ASET1GEROUS RINGS IN DORVILLEIDS AND DINOPHILIDS

99

actual mechanism for this has been proposed. In Ougia subaequalis (Ouc., 1978) the pharynx may reach into

setiger 13 with the maxillae placed in setiger 6 in die retracted state. In many other dorvilleids some of the anterior

setigers also house parts ol die pharyngeal apparatus. Thus, although the division of die peristomium may

originally have had an explanation in accordance with Akesson’s hypothesis, it is difficult in light of their

dimensions to credit the accessory peristomial fibres with an important role during pharyngeal protraction in all

dorvilleid species.

Certainly, if it were later to be demonstrated that accessory peristomial fibres are present in dinophilids diey

must be regarded as rudiments or have some other function, as diey arc completely dwarfed by the strongly

developed pharyngeal bulb (Fig. 2D).

ACKNOWLEDGMENTS

I wish to thank Wilfricd Westheide (University of Osnabruck, Germany) for suggesting this line of

investigation and for being a generous host during an extended visit to his institute. The assistance of the staff at

the Station Biologique (Roscoff, France), especially that of Captain Alain Maron. during die collection of most of

the animals used in this study is greatly appreciated. Kurt OCKEI.MANN (Marine Biological Laboratory, Ilelsingpr,

Denmark) kindly furnished the specimens of Trilobodrilus. Margit Jensen (Zoological Museum, University of

Copenhagen) is thanked for the use of her Zeiss Axiophot microscope (Carlsbergfondet grant no. 468). The Danish

Natural Science Research Council provided post-doc funding for this project (grant no. 11-8808).

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OUG, E.. 1978. — New and lesser known Dorvilleidae (Annelida, Polychaeta) from Scandinavian and northeast American

waters. Sarsia , 63 : 285-303.

STORCH. V., 1968. — Zur vergleichenden Anatomic der segmentalen Muskclsysteme und zur Verwandtschalt dcr Polychaeten-

Familien. Z Morph. Tiere. 63 : 251-342.

WESTHEIDE. W„ 1985. — The systematic position of the Dinophilidae and the archiannelid problem. In : S.C. MORRIS. J.D.

GEORGE. R.Gibson & H.M. PLATT (eds). The Origins and Relationships of Lower Invertebrates. 28 : 310-326. The

Systematics Association, Oxford.

WESTHEIDE, W.. 1987. — Progencsis as a principle in meiofauna evolution. J. Nat. Hist.. 21 : 843-854.

11

The head of Maldanidae polychaetes

of the subfamily Maldaninae

Karen D. GREEN

1537 Camino Corto

Fallbrook, CA, 92028, USA

ABSTRACT

The Maldaninae head and proboscis are described based on dissections of Asychis amphiglyptus , Bathyasychis cristatus.

Chirimia lobata , Maldane sarsi , Metasychis disparideniatus, Sabaco elongatus , and Sonaisa meridionalis. Consistent features

among these species include a well-developed cephalic plate with the rim divided by lateral notches, a wide and muscular

palpodc, a tri-lobed mouth, and an asymmetrical proboscis. It is suggested that the feeding structure is an axially-modified

ventral proboscis. Variable features include the development of the cephalic rim, nuchal organs, palpode, mid-dorsal keel, and

proboscis muscles.

RESUME

La tete des polychetes Madanidae de la sous-famillc des Maldaninae

La description de la tele et du proboscis de Asychis amphiglyptus , Bathyasychis cristatus, Chirimia lobata. Maldane sarsi,

Metasychis disparidentatus. Sabaco elongatus elSonatsa meridionalis a ete effectuee a partir de dissections. Les principales

caracteristiques chez ces cspeces sont la presence dune plaque cephaliquc bicn developpee avec un limbe divise par des

echancrures laterales. un palpode large et musculaire, une bouche trilobee, et un proboscis asymetrique. II est suggere que cette

structure pour ralimentation provienl d'un proboscis ventral axial modifie. Des caracteristiques variables ont etc observees sur

le developpement du limbe cephalique. les organes nucaux. le palpode. la carene medio-dorsale et les muscles du proboscis.

INTRODUCTION

The head is a key feature in the taxonomy of Maldanidae polychaetes. The subfamily Maldaninae

(Arwidsson, 1907; Light, 1991) is characterized as having a cephalic plate, which refers to the dorsal surface of

the head being edged by a raised rim. The cephalic rim is divided by lateral notches into a single posterior border

and paired lateral borders. The prostomial palpode is anterior to the plate. Paired nuchal organs occur on the

dorsal surface of the plate immediately behind the palpode. A keel (= carina, intemuchal ridge, median ridge)

refers to a medially raised area between the nuchal organs that may or may not extend into the posterior cephalic

border.

Historically, the height and length of the keel was used in keys to separate the Maldaninae genera Asychis and

Maldane (e.g., Arwidsson, 1907; Fauchald, 1977). However, interpretation of whether the keel is short and

Green, K.D.. 1994. — The head of Maldanidae polychaetes of the subfamily Maldaninae. In: J.-C. Dauvin, L. LAUBIER &

D.J. Reish (Eds), Actes de la 4eme Conference intemationale des Polychetes. Mem. Mus. natn. Hist. nat.. 162 : 101-109. Paris

ISBN 2-85653-214-4.

Source : MNHN. Paris

102

THE HEAD OF MALDANINAE POLYCHAETES

low, or long and high may be difficult (FauchaLD, 1972: note, keel referred to as palpode). In his revision of die

Maldaninae, Light (1991) considered oilier head features to be of generic importance; i.e., palpode shape, nuchal

organ shape, and the development and shape of the lateral borders of the cephalic rim (= lobes, margins) including

the degree offusion or separation of them from the palpode.

In contrast to die above features, the mouth and proboscis have received little attention. Arwidsson (1907)

characterized die maldanin proboscis as being fairly uniform in width, but with a short plate-like bladder at the

base, and lacking papillae. OkRHAGE (1973) histologically examined die foregut of Asychis biceps and

characterized it as a culicularized ventral sac (with an underlying muscle bulb) beneath a ciliated esophagus. He

considered these features to be consistent with Dales (1962) ventral proboscis category.

Muscles concerned with die operation of die maldanin proboscis have not been described. The only available

information concerns the maldanid subfamily Euclymeninae (Pilgrim, 1966; Kudenov, 1977), which have an

axial proboscis (Ullman & Bookhout, 1949; Dales, 1962; Pilgrim, 1966; Orrhage, 1973; Kudenov, 1977;

TZETUN, 1991). In euclymcnins, two paired groups of muscles function as proboscis retractors. The largest set

includes the retractor sheath, which inserts on die cuticularized buccal area; and the gular membrane, which

inserts on the ciliated esophageal area (sometimes referred to as pharynx). The retractor sheath and gular

membrane arc considered derivatives of a single septum; dicir origin on die ventrum marks the boundary between

the head and thorax (Pilgrim, 1966). The smallest set of muscles, termed the accessory buccal retractors, insert

on the anterior portion of die buccal region (KUDENOV, 1977; PILGRIM, 1966).

The purpose of diis paper is to provide additional information about die maldanin head and to describe the

foregut and its musculature. Consistency and variability of head features within the subfamily are addressed by

examination of representatives of Maldaninae genera recognized by GREEN (1987) and LIGHT (1991): Asychis,

Chirimia , Maldane. Metasxchis , Sctbaco , and Sonatsa.

MATERIALS AND METHODS

Non-type specimens were examined from the Allan Hancock Foundation (AIIF) in cooperation with the Los

Angeles County Museum of Natural History, and from the author's collection. Material included: Asychis

amphiglyplus, Antarctica, Hope Bay, 3. 5-7. 5 m, Staten Island station 46-63 (original label as Maldane sarsi)

(AIIF); Bcithyasychis cristatus, South America, Peru-Chile Trench, 8°43'S, 80°40'W, 3,939 m, Anton Bruun

station AB1 1-168 (original label as Sonatsa meridionalis) (AIIF); Chirimia lobata: Southern California, San

Diego Trough, 32°25,-26°0,N, 1 17°26.8'-1 17°28.LW. 1208-1244 m, trawl, Rokop station 71-45 (original label as

Asychis lobata) (AIIF); Maldane sarsi. Arctic Alaska, 71°09.8’N, 15r09.3’W, 45 m (donated by II. JONES);

Maldane cL sarsi, southern California, Santa Monica Bay, 184 m (donated by L. Harris); Metasychis

disparidentatus , southern California, Newport Beach, 100 m (donated by L. Lovell); Sabaco elongatus, northern

California, San Francisco Bay (donated by M. Wicksten); Sonatsa meridionalis , South America, Peru-Chile

Trench, 8°38'S, 80°40'W, 3,590-3,479 m, trawl, Anton Bruun station AB1 1-165 (AIIF). Representatives of all

examined species are retained in the AHF.

Terminology used by Pilgrim (1966) and Kudenov (1977) to describe heads of euclymenins is largely

adopted. However, their use of the term pharynx for the ciliated portion of the proboscis is not followed. T his is

because the term pharynx has been variously defined as a muscular portion of the proboscis (Dales, 1962) or as

die entire stomodeal region involved in the uptake of food (Purschke. 1988). Here, the proboscis is considered

the protrusile part of the gut; I refer to the culicularized portion as the buccal mass, and the ciliated portion as die

esophagus.

Nuchal organ shape is described with reference to stems and tips. The stem is the end most posterior on the

head; the tip is anterior. In the case of recurved nuchal organs, the stem is alongside die internuchal area, and die

tip curves away.

Internal features were studied dirough dissections; a sagittal cut was made dirough the head and at least the

first setiger. Drawings were made using a drawing tube fitted to a dissecting microscope. The surface of die

foregut was characterized as cuticularized (i.e., same appearance as the external integument) or ciliated (i.e.,

finely textured or granular appearance). The presence or absence of cilia was confirmed by examining slide

preparauons of each type of surface using a compound microscope.

Features identified in die figures arc abbreviated, as follows:

A = aboral annulus; ABR = accessory buccal retractors; BM = buccal mass; B.H/T = boundary of head and

K. D. GREEN

103

FlGc' A~ Ven?I1Vr,0f he?d and firsl lh0racic segmenl; B- ven,ral view- proboscis partially retracted;

„mK“ Proboscis everted; D, lateral view, proboscis everted. Asvchis amphiglyptus : E. ventro-latcral view

Eal view wS eVeh ‘ S3nlC ViT aS 1,1 E‘ bU‘ Wi,h ,,1,c,-vcn[ral cut and right side folded back; G. internal ventro-

foreeut anlf™ ,?P g P”rl!°" °f proboscis removed; H. ventral view of G. Maid, me sarsi: I, lateral view with

exoosed vl T exposed; J, ventral view of transverse cm made dorsal to retractor sheath; K, dorsal view of head

abbreviation^ ^ CU L N°‘C: not al1 blood vcssels are showi'- See Materials and Methods for definition of letter

Source :

104

THE HEAD OF MALDANINAE POLYCH AETES

thorax; BEJ = bucco-esophageal junction; CG = cerebral ganglion; CM = circular muscle; CNC =

circumesophagcal nerve connective; DBV = dorsal blood vessel; DM = dorsal mesentery; DV = dorsal valve; E =

esophagus; GM = gular membrane; GMO = gular membrane origin; INM = internuchal muscle; K = keel; LL =

lower lip; LB = lateral border; LM = longitudinal muscle; OM = oblique muscle; M = membrane; MS = muscle

strands; NO = nuchal organs; P = palpode; PB = posterior border; POC = paroesophageal cavity; RB V = retractor

blood vessel; RS = retractor sheath; SP = septum; TM = transverse muscle; UL = upper lip; VB V = ventral blood

vessel; VNC = ventral nerve cord; VS = ventral sac.

RESULTS

Head/f/iorax Boundary. The head extends from the prostomial palpode to the first complete annulus (Fig. 1 A-

D), which includes the ventral origin of the retractor sheath and gular membrane (Fig. IE). The prostomial

palpode is fused to the peristomium, which is ventrally biannulate. A ventro- lateral groove, anterior to the

bifurcation of die nerve cord, separates the mouth from an aboral annulus (Fig. 1 A). The first complete annulus

and the following setous one form die first biannulate thoracic segment, whose posterior boundary is marked by a

septum (e.g.. Fig. 2B).

Cephalic Rim. The cephalic plate has smooth borders in most of die examined species, but they are serrate in

Chirimia lobata and Mctasychis disparidentatus (Fig. 2, dorsal views). The transition between the palpode and

lateral margins is gradual in Sonatsa elongatus, marked by shallow notches in Asychis amphiglyptus ,

Bathyasychis cristatus and Maldane sarsi , or marked by clefts in Chirimia lobata and Metasychis disparidentatus.

Palpode. The palpode is as wide or wider than the mouth in all examined specimens (e.g.. Fig 1 A). The shape

of die palpode complements die shape of die plate (Fig. 2, top views). That is, the palpode is rounded and nearly

the same width of the rounded plate in Asychis amphiglyptus , Bathyasychis cristatus, Chirimia lobata , and Sabaco

elongatus. In contrast, the palpode is spade-shaped and less than 75 % the width of die elongate plate in

Metasychis disparidentatus, Maldane sarsi , and Sonatsa meridionalis. The palpode is upturned in Chirimia

lobata , conical in Sonatsa meridionalis, and angular in profile in die other species. The palpode is muscular

(Fig. 2, sagittal views); transverse muscle development is greatest in Sonatsa meridionalis (Fig. 2B).

Nuchal Organs. The nuchal organs differ in shape and length (Fig. 2, top views). Nuchal organs with nearly

parallel stems have lips that diverge or slightly curve as in Maldane sarsi (Fig. 2A), strongly curve or bend

laterally as in Asychis amphiglyptus and Metasychis disparidentatus (Fig. 2D,F), or recurve as in Chirimia lobata

and Sabaco elongatus (Fig. 2C,G). Stems curve laterally and tips are nearly parallel in Sonatsa meridionalis (Fig.

2B). 'fhe stems and tips both diverge in Bathyasychis cristatus (Fig. 2E). Nuchal organs tire reduced (< 1/6 head

length) in Sabaco elongatus ; short (1/6 to 1/3 head length) in Bathyasychis cristatus, Metasychis disparidentatus,

Maldane sarsi, and Sonatsa meridionalis ; and of moderate length (1/3 to 1/2 head lengdi) in Asychis amphiglyptus

and Chirimia lobata.

Behind the cerebral ganglion and beneath the nuchal organs is a concentration of transversely oriented muscle

bundles, herein termed die internuchal muscle (Fig. 2, sagittal views). This muscle is least developed in Sabaco

elongatus (Fig. 2C) and most developed in Chirimia lobata (Fig. 2G). The length of the internuchal muscle

approximates that of the nuchal organs in Bathyasychis cristatus, Maldane sarsi, and Sabaco elongatus ; the

nuchal organs are slightly longer than the internuchal muscle in Asychis amphiglyptus, Chirimia lobata , and

Metasychis disparidentatus. Keel development obscures die dorsal boundary of die internuchal muscle in Sonatsa

meridionalis (Fig. 2B).

Keel. The keel is convex, long, narrow, and firm in Maldane sarsi and Sonatsa meridionalis (Figs. 2A,B).

These keels are supported by multiple layers of transverse muscle bundles that extend from the palpode to die

posterior border of the plate. However, thedevelopment of the keel muscle differs between diese species. The

transverse muscle bundles tire interspersed within a dense layer of longitudinal muscle in Maldane sarsi. In

contrast, dense aggregations of transverse muscle occur below a layer of longitudinal muscle in Sonatsa

meridionalis.

Most of the odier species have slightly convex (Metasychis disparidentatus and Sabaco elongatus ) to flat

(Asychis amphiglyptus and Chirimia lobata) keels that are marked by a single layer of transverse muscle bundles,

die extent ol which corresponds to keel length. These keel are relatively narrow and compressible (loses shape

when pressed). The keel is relatively wide and firm in Bathyasychis cristatus (Fig. 2E). The firmness probably

reflects a bulging of die proboscis; diere is little space between the esophagus and the inner wall of die head.

Mouth. All examined specimens have a transverse opening and a medially incised upper lip; die lower lip has

K. D. GREEN

105

Fig. 2. Sagittal and dorsal views of heads: A. Maldane sarsi; B, Sonatsa meridional is ; C. Sabaco elongatus ; D, Asychis

amphiglyptus\ E, Bathyasychis cristatus\ F. Met asychis disparidentatus ; G. Chirimia lobata. Notes: All sagittal and dorsal

views, respectively, drawn at same scale; scale for each view shown in Fig. 2A. Equivalent features in all sagittal views

have same shading pattern, see Fig. 2B for detailed labeling. Not all blood vessels and oblique muscles are shown. See

Materials and Methods for definition of letter abbreviations.

Source MNHN , Paris

106

THE HEAD OF MALDANINAE POLYCHAETES

several longitudinal folds (e.g., Fig. 1 A).

Proboscis. Of the examined material, one specimen o t' Maldane has a fully everted proboscis (Fig. 1C-D), and

one specimen of Asychis has a partially everted proboscis (Fig. 1E-F). The proboscis consists of a cuticularized

buccal mass and the anterior part of the ciliated esophagus. The everted part of the esophagus is cushion-shaped;

the everted buccal region is asymmetrical with abasal extension (herein termed ventral sac).

In the retracted state, the proboscis is similar among the examined species (Fig. 2, sagittal views). The

cuticularized region is smooth and slightly folded. Part of it extends from the edges of the upper lips to the

esophagus. Another part infolds from the comer of the mouth and forms the ventral sac below the esophagus (Fig.

1 J-K; Fig. 2, sagittal views).

Transverse muscle may occur beneath die retracted ventral sac. This muscle is relatively well-developed in

Bathyasychis cristatus and Sonatsa meridionalis (Figs. 2B,E), is present in Asychis amphiglyptus and Chirimia

lobata (Figs. 2D,G), and is reduced in Metasychis disparidentatus, Maldane sarsi , and Sabaco elongatus (Figs.

2A.C,F).

The proboscides also differ widi regard to how folded the esophagus is when retracted. The folds are taken

here as an indication of proboscis volume; given this, the largest volume proboscides were noted for Bathyasychis

and Sonatsa.

Proboscis Retractors. On each side of the head, the gular membrane and retractor sheath originate along a path

from the head/thorax boundary towards the level of the lateral notches (Fig. 10-1). From there, the origin of the

gular membrane continues dorsally and anteriorly to the end of the plate. The retractor sheath divergesventrally.

Accessory buccal retractors originate behind the cerebral ganglion and along the line of the circumesophageal

nerve connectives.

Along the origin of the gular membrane, muscular strands extend ventro-lalerally (anterior face) and a thin

membrane extends dorso-latcrally (posterior face) (Fig. II). The muscular part of the origin ends behind the

intemuchal muscle; the membranous part continues anteriorly beneath the internuchal muscle to the dorsal valve

(Fig. 1 1 1-I). The gular membrane inserts on the ciliated esophagus.

This is reversed for the retractor sheath, which has muscular strands on the posterior face and a thin membrane

on the anterior face (veniro-lateral). The retractor sheath inserts on the cuticularized ventral sac and the line of

insertion continues towards the posterior corner of the upper lip (Fig. II).

Accessory buccal retractors lack an obvious membranous sheet, and the muscle strands insert on the buccal

mass nearest the mouth. They are most developed dorso-laterally. and slightly overlap the retractor sheath near

the comer of the mouth. Ventrally, they are less developed; they insert on the ventral buccal mass, but were not

observed where the retractor sheet inserts.

DISCUSSION

Maldaninae is one of the seven subfamilies of Maldanidae: Clymenurinae, Euclymeninae, Lumbriclymeninae,

Maldaninae, Nicomachinae, Notoproctinae, and Rhodininae (Arwidsson, 1907; Detinova, 1985a; Imajima &

Shiraki, 1982). Most subfamilies were established on, the basis of the head and pygidial regions and setal

structure, although glands were used to establish Clymenurinae (Imajima & Shiraki, 1982). The key head feature

has been whether or not the head is modified as a plate.

Results suggest additional head features that may be useful at die subfamily level. The examined specimens

shared the following features in common. The head includes a fused prostomium and peristomium, and the

peristomium is biannulate. The palpode is muscular and at least as wide as the mouth. The mouth is trilobed with

a transverse fissure and medially incised upper lip. Further, all species have an asymmetrical axially-modified

ventral proboscis. These features are discussed further below.

The composition of the maldanid head has been controversial, but it is agreed that the prostomium and

peristomium arc fused (Pilgrim, 1966; Light, 1991). Pilgrim (1966) considered the peristomium of some

euclymenins to include an additional fused segment based on the ventral accessory buccal retractors' origin, which

she associated with an aboral groove on the ventrum. In maldanins, the ventral origin of these muscles is

associated with the nerve connectives rather than the aboral groove. Further, the line oforigin is interrupted by the

retractor sheath, and the accessory retractors lack an obvious membrane. For these reasons, I interpret the aboral

groove as indicative of a biannulate peristomium rather than a septum.

Palpode development and mouth shape need further assessment in maldanids. Instead of a wide muscular

palpode, as in maldanins, some euclymenins have a muscular palpode that is narrower than the mouth (Pilgrim,

K. D. GREEN

107

1966). However, information about the extent and musculature of the prostomial palpode is lacking for most

maldanids. Narrow palpodes are common in clymenurins and cuclymenins, and indistinct palpodes arc common

in the other subfamilies (Imajima & Shirakl 1982). A tri-lobed mouth, as in maldanins, may be unique. Other

maldanids have a transverse or longitudinal fissure (Imajima & Shiraki, 1982; Kudenov, 1977; Pilgrim, 1966;

TZETLIN, 1991); however, since mouths arc rarely mentioned, this feature needs additional study.

Maldanin proboscides appear to differ from the few available reports for other maldanids. ORRHAGE (1973)

characterized Asychis biceps as having a ventral proboscis because a cuticularized ventral sac (with an underlying

muscle bulb) occurs below the ciliated esophagus. He stated that the ventral sac and muscle bulb were less

voluminous in this species than in other species with ventral proboscides; i.e., Nicomache lumbricalis

(Nicomachinae) and Rhodine gracilior (Rhodininae), but further detail was not given. Results indicate that the

ventral sac is common in maldanins, but the development of the underlying transverse muscle (bulb) is variable.

Based on TZETLlN's (1991) illustrations of Nicomache lumbricalis , Nicomache minor , and Praxillura longissima

(Lumbriclymeninae), my impression is that the muscle bulb (ventral pharyngeal organ) is less developed in

maldanins. Further die configuration of die maldanin proboscis differs from the ventral proboscides of Nicomache

minor and Praxillura longissima. In those species, die non-ciliated region primarily is a ventral structure and the

ciliated region primarily is dorso-lateral. In contrast, die non-ciliated region of die foregut is developed bodi

dorsally and ventrally in maldanins. but it forms a narrow sac ventrally.

Because the non-ciliated and ciliated regions evert as a tube-like structure in maldanins, there is some

similarity to die axial proboscides of cuclymenins (Dales, 1962; Pilgrim, 1966; Kudenov, 1977; Tzetlin,

1991). However, the ventral sac at die base of die maldanin proboscis gives it an asymmetrical appearance. This

difference in the ventral development of die proboscis is reflected in the proboscis musculature. In euclymenins,

the gular membrane and retractor sheadi share the same origin (Pilgrim, 1966; Kudenov, 1977). In maldanins,

the retractor sheath diverges and follows a more ventral course. Furdier, accessory buccal retractors, which are

well-developed in euclymenins, tire mainly dorso-lateral in maldanins and only weakly developed ventrally

(presumably due to die ventral padi of the retractor sheadi).

Accordingly, results suggest that maldanins have a axially-modified ventral proboscis. The axial modification

refers to the tube-like appearance of the everted proboscis. However, because die appearance of the tube is

asymmetrical (due to the ventral sac), the retractor sheath is ventrally oriented, and a muscle bulb may be present,

I consider the structure more consistent widi the ventral proboscis category. TZETLIN (1991) provides a hypothesis

of proboscideal evolution within die order Capiteliida in which the ventral state is considered more primitive than

die axial state. Perhaps the axially-modified ventral proboscis of maldanins represents an intermediate state in

Tzetlin's (1991) hypothesis.

Within Maldaninae, several features are variable. Because this study only compares a single representative of

each genus, it is not possible to comment on consistency of features within each genus. However, results do

permit some comment regarding features considered of generic importance, and docs suggest other features dial

may be promising to investigate.

With regard to the cephalic rim, Light (1991) considered the development and shape of the lateral borders and

their separation from the palpode as a generic feature. An additional characteristic that may contribute to

descriptions of tliis feature is die development of die notch or cleft that may separate die borders and palpode.

Light (1991) recognized three shapes of Maldaninae palpode; spade-like, mushroom-shaped, and indistinct.

Results indicate that shape categories are variable within some genera. For example. Light characterized die

palpode of Asychis as spade-like, and that of Metasychis as mushroom-shaped; however, the examined Asychis

amphiglyptus has a rounded palpode, and the examined Metasychis disparideniatus has a spade-like palpode. It is

suggested that descriptions of shape may be improved by considering die profile and thickness of die palpode.

Light (1991) characterized maldanin nuchal organs as four basic shapes (J-shaped, U-shaped, slightly curved,

and crescentic). Additional categories are needed to describe nuchal organs in which the stems diverge (as in

Sonatsa) and in which both stems and tips diverge (as in Bathyasychis). It is suggested that descriptions of nuchal

organs include reference to stem and tip shape and lengdi. The internuchal muscle appears to relate to

characteristics of die nuchal organs (e.g., shape and length), and additional study of this muscle is warranted. The

internuchal muscle, which may be prominent in maldanins, has not been investigated for oilier maldanids.

A cephalic keel, though not considered a generic character by LIGHT (1991), was considered so in the past.

Results indicate that the usefulness of the keel as a taxonomic character may be improved by taking into

consideration compressibility and width when evaluating the more traditional height and length characters.

Examinations of muscle development provides a means to cross check keel designations.

108

THE HEAD OF MALDANINAE POLYCHAETES

Features of tlie proboscis vary among the examined species. Baihyasychis and Sonatsci are similar in having

the densest concentrations of transverse muscles beneath the ventral sac, and the largest volume proboscides of

the examined species. It is not known whether these similarities are due to feeding in a similar environment (both

co-occur at abyssal depths in trenches) or close phylogenetic relationship. Because both taxa have nuchal organs

with diverging stems (the tips also diverge in Baihyasychis ), another feature suggests relationship.

In die past it was questioned whether Sonatsa was distinct from Maldane since they arc morphologically

similar (Arwidsson, 1922: Detinova, 1985b). GREEN (1987) argued for recognition of Sonatsa based on nuchal

organ shape and the presence of an enlarged ventral glandular pad on setiger 5. The similarities in proboscis

development mid nuchal organs between Baihyasychis and Sonatsa support Sonatsa' s generic status. So do the

differences between Sonatsa meridionalis and Maldane sarsi in die muscle development of the proboscis, keel,

and palpode.

Other species provide an additional example where similarity in external morphology does not correspond

with proboscis musculature. For example, Chirimia lobata and Metasychis disparidentatus have serrate cephalic

borders: however, the development of the muscles beneath the ventral sac differ. Proboscis muscles are more

similar between Chirimia lobata and Asychis amphiglyptus ; diese species also arc similar in having well-deve¬

loped intemuchal muscles. Conversely, die appearance of the plaque differs among Metasychis disparidentatus ,

Maldane sarsi , and Sabaco elongatus, but diey are similar in having reduced ventral sac muscles. The intemuchal

muscle is similar between Metasychis disparidentatus and Maldane sarsi , but is unique in Sabaco elongatus.

Although it is not known at this time which features are more reflective of convergence or relationship, this

study supports die status of die genera. It also supports the view that important features include die development

of the cephalic rim and nuchal organs. I suggest that proboscis musculature, keel development, and palpode shape

may be important, but need further study.

ACKNOWI JUDGEMENTS

Special thanks go to Leslie II arris of the Allan Hancock Foundation for the loan of specimens. Larry Lovell

generously allowed use of his microscope with drawing tube. Discussions widi Dr. Kirk FlTZHUGH prompted me

to prepare diis paper, and I appreciate his interest. I am grateful to Drs. Jerry Kudenov, Alexander TZETLIN, and

two anonymous reviewers for dieir comments to an earlier draft of diis paper.

REFERENCES

Arwidsson, I.. 1907. — Studien liber die skandinavischen und arktischen Maldaniden nebst Zusammenstellung der iibrigen

bisher bekannten Arten dieser Familie. Zool. Jhrb., Suppl., 9 : 1-308.

Arwidsson. I., 1922. Systematic notes on some maldanids. Svenska Vetensk. Akacl. Stockholm, Hand., 663 : 1 -46.

Dales, R.P.. 1962. — The polychacte stomodeum and the inter-relationships of the families of Polychaeta. Proc. Zool. Soc.

bond ., 139: 389-428.

Detinova. N.N.. 1985a. Taxonomy, composition and distribution of polychaetes of the subfamily Lumbriclymeninae

(Maldanidae). hr. Polychaeta: Morphology, syslematics, ecology. Proc. USSR Polychaeta Conference. Leningrad. 1983 :

25-29. (in Russian].

Detinova, N.N., 1985b. The taxonomic significance of the structure of the parapodia in some Maldanidae (Polychaeta).

Zool. Zh., 64 : 1487-1492. (in Russian].

FAUCHALD. K.. 1972. — Benthic polychaetous annelids from deep water off western Mexico and adjacent areas in the eastern

Pacific Ocean. Allan Hancock Monogr. mar. Biol., 7 : 1-575.

Fauchald. K., 1977. — The polychaete worms: Definitions and key to the orders, families and genera. Nat. Hist. Mus. Los

Angeles County, Sci. Ser., 28 : 1-190.

Green, K.D., 1987. - Revision of the genus Sonatsa (Polychaeta: Maldanidae). Bull. Biol. Soc. Wash., 7 : 89-96.

IMAJ1MA, M. & Y. SiriRAKI, 1982. Maldanidae (Annelida: Polychaeta) from Japan (Part 1,2). Bull. Nat. Sci. Mus., Tokyo,

8 : 7-88.

K. D. GREEN

109

Light, W.J.H., 1991. — Systematic revision of the genera of the polychaete subfamily Maldaninae Arwidsson. Ophelia

Suppl. , 5 : 133-146.

ORRHAGE, L.. 1973. Two fundamental requirements for phylogenetic-scientific works as a background for an analysis of

Dale’s (1962) and Webb’s (1969) theories. Z. Zool. Syst. Evolut.-forsch., 1 1 : 161-173.

PILGRIM, M.. 1966. — The morphology of the head, thorax, proboscis apparatus and pygidium of the maldanid polychaetes

Clymenella lorquata and Euclymene ocrstedi.J. Zool., Land., 148 :453-475.

PURSCHKE, G.. 1988. — XI. Pharynx. In W. WESTHEIDE & C. O. HERMANS (eds), The Ultrastructure of Polychaeta.

Microfauna Marina . 4 : 177-197. Gustav Fischer Vcrlag, Stuttgart, New York.

TZETLIN, A.B. 1991. — Evolution of feeding apparatus in the polychaetes of the order Capitellida. Zool. Zh 70 : 10-22. [in

Russian].

ULLMAN. A. & C.G. BOOKHOUT. 1949. — The histology of the digestive tract of Clymenella lorquata (Leidy). J. Morph., 84 :

31-55.

Source : MNHN. Paris

12

Effects of sample fixation on body shape of

Capitella capitata (Polychaeta, Capitellidae)

Marfa Nuria MENDEZ & Marfa Jose CARDELL

Departament d’Ecologia, Facultat de Biologia

University of Barcelona

Avda. Diagonal 645

08028 Barcelona Spain

SUMMARY

Formaldehyde fixed specimens of Capitella capitata from the littoral zone of Barcelona showed several body forms :

"contracted C. capitata" (CC) - pointed proslomium. contracted thorax, anterior setigers distinct; "elongated C. capitata"

(EC) - triangular prostomium/peristomium, elongated thorax, anterior setigers indistinct; "intermediate C. capitata" (IC)

- intermediate form between CC and EC. Five fixation tests were performed using different formaldehyde concentrations,

sieving or unsieving before fixation, and different periods between sample collection and fixation. By these tests it was

shown that CC is the regular form, whereas EC and IC are caused by deficiencies in sample fixation. Recommendations are

given for avoiding the fixation aberrant fixation forms which might impair studies in taxonomy and population

dynamics of this species.

RESUMfi

Effets de la fixation dcs ecliantillons sur la forme du corps dc Capitella capitata (Polychaeta,

Capitellidae)

Des specimens preserves de Capitella capitata du littoral de Barcelone monlrent plusieurs formes du corps : "C.

capitata contractee" (CC) - prostomium poinlu, thorax comrade, seligeres anterieurs bien differences ; "C. capitata

allongee (EC) - prostomium/peristomium triangulaire. thorax allonge, seligeres anterieurs pas differencies ; "C. capitata

intermediate (IC) - forme intermediate entre CC' et EC. Cinq experiences de fixation out ete cffectuces avec differentes

concentrations de formol, lamisage el pas de lamisage des (Schantillons avant la fixation el differentes periodes dc temps

entre le prelevement et la fixation. Lcs resultals indiquent que CC esl la forme reguliere. landis que EC el IC sont le resultat

des imperfections de la fixation des echantillons. On propose plusieurs recommandalions pour eviter les formes

aberrantes comme consequence du procede de Fixation qui peut contrarier les etudes de systematique et de dynamique des

populations de cette espece.

INTRODUCTION

Eraditional procedures for treating soft-bottom samples to obtain benthic macrofauna were given, among

MENDEZ. M.N. & M J. CARDELL, 1994. — Effects of sample fixation on body shape of Capitella capitata (Polychaeta.

C apitellidae). In: J.-C. DaUVIN, L. LAUBIER & D..I. REISH (Eds). Actcs de la 4eme Conference internationale des

Polychetes. Mem. Mus. natn. Hist. nat.. 162: 111-117. Paris ISBN 2-85653-214-4.

Source : MNHN. Paris

M.N. MENDEZ & M.J. CARDELL

others, by Banse & Hobson (1974), Fauchald (1977), and ELEFTHERiou & Holme (1984). Those techniques

include screening and fixation of samples which may cause alterations to the organisms such as contraction or

damage to soft-bodied animals. Degrees of contraction may vary in some organisms and therefore, changes arc

unpredictable and possibly resulting confusions in identifications.

In previous studies of benthic macrofauna from the littoral zone of Barcelona several body forms of preserved

specimens of Capitella capitatci (Fabricius, 1780) were observed (ROS et cil. , 1990: Ros & CarDULL, 1991:

Flos & Serra, 1992). The different body shapes are found in the same preserved sample and which have not been

distinguished in live specimens. This suggests that treatment of samples may modify the body form of this

species thus impairing taxonomy and population dynamics research. In view of future studies ii is of interest to

determine which sample treatments may produce changes in die body shape of C. capitaia .

MATERIAL AND METHODS

Bottom samples were collected by SCUBA diving from the upper 10 cm of sediment near the Olympic Harbour

of Barcelona (15 m depth) between February and May 1992. The sediment in this site was fine sand (0.125 - 0.250

mm).

Five different tests were designed to evaluate single and combined effects of the following variables of fixation:

formaldehyde concentration, screening of samples and time between collection and fixation of samples.

'Lest 1. — Formaldehyde concentration.

Live specimens were sorted from the sediment and submerged in 1 1 different solutions of formaldehyde in sea

water (from 0.1 to 4%).

Test 2. — Formaldehyde concentration mid screening of samples.

Twenty samples of sediment were collected. The combined effect of die following two variables was tested:

sieving (through a 0.5 mm mesh) or unsieving samples before fixation and formaldehyde concentration (1 and

4 %). Five replicates from each combination were obtained.

Test 3. — Time.

Sixteen samples of sediment were collected. The combined effect of the following three variables was tested:

sieving (0.5 mm) or unsieving samples before fixation, formaldehyde concentration (1 and 10%) and time between

collection and fixation (0. 2, 4 and 6 hours).

In both test 2 and lest 3, sieved samples consisted of 125 ml of sediment and 62.5 ml of seawater, while

unsieved samples consisted of 250 ml of sediment and 125 ml of seawater. The different formaldehyde

concentrations were calculated according to the volume of the overlying water by the addition of concentrated

formaldehyde.

Test 4. — Presence of sediment.

Each of 100 live specimens was transferred to separate jars with 2 ml of a 4% formaldehyde solution, and each

of 100 live specimens was covered by a 3 mm layer of fine sand and fixed by the addition of 2 ml of a 4%

formaldehyde solution.

Test 5. — Volume of sediment.

Five samples of different volumes of sediment were placed and fixed with a 4% formaldehyde solution inside

cylindrical sample jars of several sizes wich were turned several times. After 24 hours of sedimentation, each

sample was divided in three horizontal layers and each level was analyzed separately.

Individuals of the different body shapes were counted in all the tests. A two way ANQVA test and Pearson's

correlations were performed to assess the effect of these variables on the body shape of C. capitatci.

RESULTS

Three different body forms of C. capitatci were distinguished according to their thorax shape. They were called

"contracted C. capitatci " (CC). "enlarged C. capitatci " (EC) and "intermediate C. capitatci " (IC). CC has a rather

pointed prostomium partially withdrawn back into die contracted first setiger, indistinct peristomium and thoracic

setigers are strongly distinct (wider than they tire long). EC presents a prostomium and peristomium widi a

broadly rounded triangular shape, thoracic setigers indistinct (slightly broader than they are long) and a slender

thorax. IC presents an intermediate thorax shape between CC and EC and has a rather pointed prostomium

partially withdrawn

Source : MNHN. Paris

SAMPLE FIXATION AND BODY SHAPE IN CAPITELIA CAP FT AT A

113

Fig. 1. — Anterior end of “contracted Capitella capitata" (CC): a. dorsal view (female), b. lateral view (male), c, lateral

view (juvenile). Anterior end of "elongated C. capitata" (EC): d, dorsal view (male), e, lateral view (female), f. lateral

view (juvenile). Anterior end of “intermediate C. capitata" (IC): g. lateral view (male).

Source : MNHN , Paris

114

M.N. MENDEZ & M.J. CARDELL

back into the contracted first setiger, indistinct peristomium, and thoracic setigers slightly distinct (slightly broader

than thev are long) (Fig. 1). .

Since CC was dominant form in the samples, results only show frequency of EC and IC which were considered

as the modified forms.

Test 1 . — Formaldehyde concentration.

Relative abundances of IC increased with low concentrations of formaldehyde (<0.2%) (Table 1). EC did not

occur. Therefore, individuals which are fixed with low concentrations of formaldehyde probably die slowly and

relaxed thus producing die characteristic enlargement of thorax from IC. This agrees with the suggestion given by

BaNSE & HOBSON (1974) about a relaxed state of animals obtained with few drops of concentrated formaldehyde

in 1 litre of sea water.

Table 1. — Frequency of “elongated Capitella capitata" (EC) and "intermediate C. capilaia" (1C)

at various formaldehyde concentrations (F.C.). N = total number of C. capilaia.

Test 2. — Formaldehyde concentrations and screening of samples.

EC was only present in unsieved samples. Its relative abundance was slightly higher at 1% than at 4%

formaldehyde (Table 2).

The two way anova test showed a significant difference in the relative abundance of EC on sieved/unsieved

samples (F= 10.206, p= 0.006). No significative differences were obtained related to formaldehyde concentrations

(F= 1.506, p= 0.238).

The unsieving procedure seems to be the most important factor to obtain higher quantities of EC.

Nevertheless, a slight formaldehyde concentration effect was observed.

Table 2. — Frequency of “elongated Capitella capilaia" (EC) in sieved and unsieved samples fixed with

1 % and 4 % formaldehyde. Total number of C. capilaia between brackets.

Source :

SAMPLE FIXATION AND BODY SHAPE IN CAPITELLA CAP/TATA

115

Test 3. — Time.

When fixation was performed directly after sampling, EC was only present in unsieved samples (as in test 2).

Nevertheless, when fixation was performed later, EC appeared in sieved and unsieved samples. The relative

abundance was not always higher in unsieved samples. No significative correlations were observed between time

and the other tested variables (Table 3).

Table. 3. — Frequency of “elongated Capitella capitata" (EC) in sieved and unsieved samples Fixed with

1% and 4% formaldehyde at different times after their collection. Pearson’s correlations (r) are calculated

between time and frequency of EC obtained for each procedure. Total number of

C. capitata betwenbrackets. F.C. = formaldehyde concentration.

Depletion of oxygen in sediments has been reported to cause the organisms to crawl near die sediment surface

(Banse & Hobson, 1974). Results obtained in tests 1 and 2 suggest diat lower quantities of EC could result in

samples fixed several hours alter their collection than in samples fixed directly after sampling. Hence, a higher

percentage of individuals wich have a CC shape could be expected when samples are fixed after several hours due to

the upward migration of individuals and the impact of a formaldehyde concentration near to 40 %. However, our

results did not confirm this hypothesis. It is suggested that time produces an unpredictable effect on the amount of

EC.

Test 4. — Presence of sediment.

Fourteen percent of isolated specimens fixed under sediment belonged to EC, whereas this form was not present

among individuals fixed without sediment. A thin layer of sediment, appears sufficient to change the body shape of

some individuals. This was confirmed in test 5.

Test 5. — Volume of sediment.

Results given in Table 4 show that there was a direct relationship between percentage of EC and volume of

sediment inside a jar. Also a gradient was observed: the lower layers had the highest percentages of EC.

Correlations between cumulative volumes (from upper to lower layers) and relative abundance of EC were highly

significative (r= 0.939, p< 0.01, n= 13). High frequencies of EC may be caused by compression increasing and

formaldehyde diffusion decreasing with sample volume.

Table 4. — Frequency of “elongated Capitella capitata ” (EC) in five samples of different volumes of

sediment divided in three equal layers inside a jar. Total number of C. capitata between brackets.

Results obtained in the five tests suggest that the simultaneous presence of the CC, EC and IC in a sample can

be explained by die combined effect of formaldehyde concentration and sediment. Lower formaldehyde

concentrations, during fixation, may induce organisms to change from a contracted (CC) to a more relaxed shape

116

M.N. MENDEZ & M.J. CARDELL

(EC) The combined effect of sediment and formaldehyde in an unsieved sample inside ajar may be explained due

to the thickness of die sediment which can delay Hie diffusion of formaldehyde, and prolonging death. The presence

of large amounts of sediments may be responsible of an increase in the quantities of EC.

DISCUSSION

Traditional techniques used in taxonomy of polychactes are based on collection, screening (before fixation),

fixation and preservation. Neverdicless, in population dynamics studies of C. capitata, fixation is generally

performed before screening (Warren, 1976; Tsutsumi & Kikuchi, 1984; TSUTSUMI, 1987). When fixation is

performed before screening, some EC and IC may be present and thus result in errors of taxonomy and populations

dynamics:

- Taxonomy. The evident peristomium of EC can be confused with the achaetous first segment ot die genus

Capitomastus, although diere are some odier features to distinguish between both genera. This confusion has

recently been studied by WARREN (1991).

- Population dynamics. Population dynamics studies of C. capitata are performed by different thoracic

measures (Warren, 1976; Tsutsumi & Kikuchi, 1984; Tsutsumi, 1987; Martin, 1991), which may be

strongly affected by treatment of samples, so erroneous interpretations can be obtained.

CONCLUSIONS

Treatment of soft-bottom samples during fixation may affect the shape of fixed C. capitata. Body shapes were

related to different combinations of the tested variables. The elongated thorax of IC seems to be associated with

low formaldehyde concentrations. Fixation of samples widiout sieving may produce an increase in the frequency of

EC: compression and weight of sediment inside a sample jar affect die shape of C. capitata, probably because of

decreased formaldehyde diffusion and mechanically prevented body contraction.

Mistakes in taxonomy and population dynamics studies can result from inappropiate fixing procedures.

Therefore, to avoid fixation anomalies in C. capitata it is recommended:

- Sieve (he sample before fixation to avoid effects by compressed sediments. If diis is not possible, fix small

volumes of sediment (e.g. 200 ml) in several sample jars to allow die diffusion of formaldehyde and to minimize

compression.

- Ensure that fixation is done at least at 4% formaldehyde, particularly if the sample cannot be sieved before

fixation.

- Turn the sample jar several times after fixation for about 15 minutes to be certain that all the individuals have

died.

- Maintain the time between collection and fixation constant during the study.

ACKNOWLEDGMENTS

This research was supported by the Villa Olunpica, S.A., Barcelona. We are grateful to Dr. Rafael Sarda Dr.

Josep M. GlLl and Dr. Jordi FLOS for their advice and comments on the manuscript. We wish to thank Dr. Judith

GrasSLE for her constructive comments.

REFERENCES

BaNSE. K. & K. D. Hobson. 1974. — Benthic errantiate polychaetes of British Columbia and Washington. Dull. Fish.

Res. Board Can.. 185 : 1-111.

Eleftheriou. a. & H. HOLME, 1984. — Macrofauna techniques. In: N.A. HOLME & A. D. MclNTYRE (eds). Methods for the

study of marine benthos. Blackwell Scientific Publications. Oxford : 140-216.

FaUCHALD, K., 1977. — The polychacte worms. Definitions and keys to the orders, families and genera. Nat. Hist. Mus.

Los Ang. County Sci. Ser., 2 : 1-188.

Source :

SAMPLE FIXATION AND BODY SHAPE IN CAPITELLA CAP HAT A

117

Flos, J. & J. Serra. 1992. Repercusid ecoldgica i geodindmica de tes actuacions en el front marltim de llevant de

Barcelona. Informe iconic, V.O.S.A., Barcelona, 144 pp.

Martin, D., 1991. Macroinfauna de una bahfa mediterrdnea: esludio de los niveles de organizacidn de las poblaciones

de anelidos poliquelos. Doctoral Thesis. U. Barcelona, 456 pp.

ROS.J.D.. Cardell. M.J., Alva, V., Palacin, C. & I. LLOBET, 1990. — Comunidades sobre fondos blandos afectados por

un aporte masivo de lodos y aguas residuales (litoral frente a Barcelona, Mediterraneo occidental) : resultados

preliminares. Bentos 6 : 407-423.

Ros, J.D. & M.J. CARDELL, 1991. — Effect on benthic communities of a major input of organic matter and other

pollutants (coast off Barcelona. Western Mediterranean). Toxicol Environ, Chem., 31-32 : 441-450.

TSUTSUMI, H., 1987. Population dynamics of Capitella capitata (Polychaeta: Capilcllidae) in an organically polluted

cove. Mar. Ecol. Prog. Ser., 36: 139-149.

TSUTSUMI, II. & T. KlKUCHI, 1984. Study of the life history of Capitella capitata (Polychaeta: Capitellidae) in

Amakusa. South Japan including a comparison with other geographical regions. Mar. Biol., 80 : 315-321.

Warren. L.M.. 1976. — A population study of the polychaetc Capitella capitata in Plymouth. Mar. Biol., 38 : 209-

216.

Warren, L.M., 1991. — Problems in Capitellid taxonomy. The genera Capitella, Capilomastus and Capitellides

(Polychaeta). Ophelia , suppl. 5 : 275-282.

Source : MNHN. Paris

13

Ultrastructure of sense organs and the central nervous

system in Parenterodrilus taenioides and their

phylogenetic significance in the taxon

Protodrilida (Annelida, Polychaeta)

Giinter PURSCHKE * & Claude JOUIN-TOULMOND **

* Spezielle Zoo logic. Fachbereich 5

Universitat Osnabruck

D-49069 Osnabruck. Germany

** Biologie et Physiologic des Organismes Marins

Universite Pierre el Marie Curie

4. place Jussieu

F-75252 Paris Cedex 05. France

SUMMARY

The following sense organs palps, nuchal organs, and presumed unpigmented ocelli, as well as the central nervous system

were investigated by electron microscopy in Parenterodrilus taenioides . The palps are mobile sensory structures bearing motile

cilia and four types of sensory cells, including presumed phaosomous ocelli. The palp canals are small, filled with cell bodies

ol muscle cells and a few coelenchyme cells. The canals are covered by a cord of coelenchyme cells. The comparatively large

nuchal organs are identical in structure with those of the other Protodrilida. There are two types of presumed ocelli located in

posterior ganglionic expansions of the brain. The palps are innervated by three nerves originating from the dorsal and ventral

roots of the circumoesophageal connective. The most exceptional features of the brain are four ganglionic expansions

extending far posteriorly into the head segment. The lateral ones fuse with the small dorsal root of the circumoesophageal

connectives. These findings are compared with the sense organs and the nervous system of the other Protodrilida. They clearly

corroborate the supposed relationship ol the Protodrilida and additional autapomorphies demonstrate the derived position of P

taenioides.

RESUME

Ultrastructure des organes sensoricls et du systeme nerveux central dc Parenterodrilus taenioides et leur signification

Phylogenetique chez les Protodrilida (Annelidcs Polychetes)

Les organes sensoriels tels que palpcs. organes nucaux. structures assimilees a des ocelles non pigmentes, ainsi que le

systeme nerveux central ont ete etudics au niveau ultrastructural chez Parenterodrilus taenioides. Les palpes sont des appen-

PURSCHKE G. & C. Jouin-Tqulmond, 1994. — Ultrastructure of sense organs and the central nervous system in

arenterodrdus taenioides and their phylogenetic significance in the taxon Protodrilida (Annelida. Polychaeta). In:

DauviN' L. LAUBIER & D.J. REISII (Eds). Actes de la 4cme Conference internationale des Polychetes. M£m Mus naln

Hist, not., 162 : 1 19-128. Paris ISBN 2-85653-214-4.

Source : MNHN, Paris

120

G. PURSCHKE & C. JOUIN-TOULMOND

dices sensoriels cilies et mobiles qui portent quatre types de cellules scnsorielles, dont des ocelles de type phaosome. Les

canaux internes des palpes sont minces, remplis par les corps cellulaires des cellules musculaires et par quelqucs cellules du

coelenchyme qui formenl aussi un cordon cellulairc a la peripherie de chaque canal. Les palpes re^oivent trois nerfs issus des

racines dorsales et ventrales des connectifs p£rioesophagiens. Les organes nucaux, relativement larges, ont une structure

identique k ceux des autrcs Protodrilida. Deux autres types de structures, assimilecs a des ocelles non pigmentes, sont logees

dans des expansions ganglionnaires posterieures du cerveau. Les caractiSristiques les plus remarquables du cerveau sont ces

quatres expansions ganglionnaires qui s'etcndent loin vers 1’arriere, dans le segment cephaliquc. Les expansions les plus

laterales fusion nent avec les petites racines dorsales des connectifs perioesophagiens. Ces caractcrcs sont compares k ceux des

autres Protodrilides et les nouvelles autapomorphies revelees par ce travail demontrent que P. laenioides csl une forme derivee.

L'enscmble des res u I tats confirme les relations prelablement etablies au sein des Protodrilida.

INTRODUCTION

The Protodrilida are interstitial polychaetes characterized by a long and slender body, reduced or absent

parapodia, a pair of prostomial appendages (palps), and a pygidium generally with two adhesive lobes. The about

60 known species of the taxon belong to only four genera: Saccocirrus Bobretzky, 1871, Protodrilus Hatschek,

1880, Protodriloides Jouin, 1966 and Parenterodrilus Jouin, 1992. Electron microscopic investigations were

conducted to clarify the functional morphology of selected organs as well as to test the proposed monophyly of

the Protodrilida and tiieir subordinate taxa, to evaluate their relationship and to find synapomorphies with their

supposed sister group, the Spionida (e.g., PURSCHKE & Jouin, 1988; Purschkh, 1990a, 1993). In contrast to the

small body size and the apparently simple organization of these polychaetes, their sense organs and the central

nervous system turned out to be rather complex structures when investigated by electron microscopy (Eakin et

al. , 1977; PURSCHKE, 1990a, 1990b, 1990c, 1992, 1993; PURSCHKE & JOUIN-TOULMOND, 1993). Therefore, these

structures provide numerous characters which might be useful for phylogenetic considerations.

Sense organs present in every species are: the palps, the nuchal organs, and various types of unpigmented

presumed ocelli. Pigmented ocelli only occur in the Saccocirrus species and a few Protodrilus species. These

structures have now been investigated in species of every genus except the monotypic Parenterodrilus , which is

so lar only known lrom sublittoral coral sands of the island of Moorea, French Polynesia. Parenterodrilus

tcienioides is especially remarkable because it is the only known polychaete possessing a vestigial alimentary

canal, without mouth and digestive cavity (JOUIN, 1979, 1992). Thus, the main purpose of the present

investigation was to clarify die functional morphology of die sense organs and die central nervous system of this

rare species, in order to use these supplementary data for a comprehensive phylogenetic discussion of the

Protodrilida. The present findings fit very well into a dendrogram showing die presumed relationship of the

subordinate taxa of the protodrilidans which has previously been suggested (PURSCHKE & JOUIN, 1988) and which

can now be based on an even larger number of characters.

MATERIAL AND METHODS

Specimens of P. laenioides were collected by die junior author in sublittoral sands of die barrier reef at die

type locality in Moorea, French Polynesia (JOUIN, 1979). After relaxauon in a mixture of equal parts of sea water

and 7.7 % MgCl2, specimens were fixed in a cacodylate buffered (0.2 M, pH 7.4) solution of 2 % glutaraldehyde,

adjusted widi NaCI to about 1,300 mosM for 1 h. They were rinsed in die same buffer, postfixed in buffered 1%

OSO4, dehydrated in an ethanol series, and embedded in Epon. Ultrathin secdons of two specimens were cut widi

a diamond knife on a Reichert Ultracut E microtome and ribbons of sections were collected on single slot grids

coated widi piololonn support Film in order to obtain complete series of ultrathin sections. They were stained in

an

Fig. 1 A-F. Parenterodrilus laenioides. Palps. A. Low power TEM micrograph of cross section appr. 25 pm above the palp

base; center occupied by palp canal (pc) and coelenchyme cells ( coc ); palp nerves encircled; arrow points to position of

blood vessel. B. Cross section of palp canal. C. Ventral palp nerve vpnj and longitudinal muscle fibres; note disappearance

ol extracellular lamina (la) between coelenchyme and epidermal cells lateral to vpnj (small arrows ); the large arrow

points to position of palp canal. D. Tangential section of ventral side with ciliated cells ( cce ). epidermal supporting cells

(ep) and sensory cells (arrows). E. Coelenchyme cell with nucleus. F. Blood vessel (bv). - cce ciliated cell, cm circular

muscle fibre, coc coelenchyme cell, cu cuticle, dpn dorsal palp nerve, ep epidermal supporting cell, gc glial cell, gl gland

cell, la extracellular lamina, bn longitudinal muscle cell, pc palp canal, vpnj 4 ventral palp nerve 1,4.

SENSE ORGANS AND CENTRAL NERVOUS SYSTEM IN PARENTERODRILUS TAENIOIDES

121

Source : MNHN , Paris

122

G. PURSCHKE & C. JOUIN-TOULMOND

LKB Ulirosiainer and examined with a Zeiss EM 109 electron microscope. Reconstruction of (he nervous system

was done from low power electron micrographs taken at intervals of between 0.7 pm and 3.5 pm, depending on

(he structures observed.

RESULTS

In Parenterodrilus taenioides the palps arise in an anterior-lateral position from the prostomium. The filiation

of the anterior end is very well developed; in addition to numerous sensory cilia, the palps, prostomium and head

segment (= peristomium) bear mobile cilia as well. The nuchal organs are heavily ciliated, rounded areas of about

25 pm diameter at die posterior end of the prostomium. IJnpigmented ocelli are not visible with light microscopy.

Palps. The palps are circular to oval in cross section. They are composed of cuticle, epidermis, sensory cells,

intraepithelial nerves, a palp canal, a small blood vessel, and so-called coelenchyme cells (Fig. 1A-F). The

epidermis is comprised of supporting cells, with glandular and ciliated cells distributed among them. The latter are

restricted to the ventral side where they are arranged in bands. There are three palp nerves: die medial nerve

( \pti4\ see PURSCHKE, 1993 for terminology) is the largest and contains about 330 nerve fibres; the other nerves

are considerably smaller and consist of 15 ( dpn ) and 35 (vpnj) fibres. Small branches of these longitudinal nerves

form a network of nerve cell processes ventral ly, and around die palp canals. Each nerve is pardy enveloped by

glial cells (Fig. 1 B). In the nerve fibres clear vesicles widi a diameter of 40-60 nm and dense-cored vesicles of VO-

95 nm diameter are present (Fig. 1C). Neuroneuronal and neuromuscular synapses were frequently observed

within die nerve tracts.

Each palp has a small canal, 10-15 pm in diameter (Fig. 1A-C, E-F). The canals are situated ventrally in the

palps and unite behind the neuropile of the brain. They are filled widi muscle cells and a few coelenchyme cells,

surrounded by an extracellular lamina. There arc only a few small muscle fibres outside die palp canals, most of

which arc situated close to the small ventral palp nerve (vpnp. Fig. 1C). Besides these longitudinal fibres diere are

a few small circular fibres in die palp canals. The canals are covered dorsolaterally by coelenchyme cells, which

are electron-lucent with only very few organelles and an irregular outline (Fig. 1 A, C, E). Although of presumably

mesodermal origin, this coelenchyme tissue is not separated from die epidermis by a basal lamina on all sides;

extracellular material was only detectable between die palp canal and die small palp nerve (Fig. 1C). Each palp is

supplied by a small blind-ending blood vessel which is situated at die palp canal opposite to die main palp nerve.

Three types of bipolar sensory cells have been found on the palps and die prostomium (Fig. 2A-F). The

monociliary type-1 sensory cells are so-called collar receptors (e.g. Schlawny el al.t 1991): the cilium passes

through die cuticle and is surrounded by 10 modified microvilli (Fig. 2A-B). A cylinder of electron-dense material

lies below the microvilli. It is connected to die ciliary rootlet just underneadi die basal body. Proximally, thin

filaments originate from this cylinder and enter die microvilli. The dendritic processes are about 1 pm in diameter

and contain 3-4 long mitochondria (Fig. 2A). The second type of sensory cell is multiciliary, widi 3-9 cilia

penetrating the cuticle (Fig. 2C-D). These sensory cells are die most frequent; they eidier occur in isolation or

grouped in two adjacent sensory cells forming a ciliary tuft. The cilia are of different lengdis and may be up to

15 pm long. They usually arise from a slight depression of die cell apex, which creates a raised rim at die

periphery of die sensory cell (Fig. 2D). The cilia are surrounded by short microvilli and anchored by long roodets

(Fig. 2C). Sensory cells of the diird type have non-penetrative (intracuticular) cilia and diey may be isolated or

clustered in groups of up to 9 sensory cells (Fig. 2E-F). Their long dendritic processes extend above die level of

die adjacent epidermal cells and bear one or two horizontal cilia (Fig. 2E). The cilia are about 4 pm long and have

a 9x2+0 axoneme (Fig. 2E, inset). Usually they divide in branches in which the microtubules are successively

lost.

Nuchal organs. The nuchal organs consist of numerous ciliated supporting cells, an average of seven bipolar

sensory cells, and a retractor muscle (Fig. 3A-D), which runs ventromedially and attaches to die posterior end of

the palp canal. Ciliated supporting cells surround die dendritic processes of die sensory cells forming die olfactory

chamber (3.5-4 pm in diameter) in die middle of the ciliated area (Figs 3 A, 4). They bear ail average of 35 cilia

(3.2 cilia per pm2), which are anchored by basal bodies and long striated rootlets. The ciliated supporting cells

give also rise to numerous microvilli; these form a paving-stone-like cover above die cuticle, which is only

penetrated by die cilia of diese cells (Fig. 3B-C). This layer also covers the olfactory chamber. The dilated

microvillar tips are cubic in shape, only 20 nm apart and interconnected by fibrillar material (Fig. 3C). Numerous

clear vesicles, coated vesicles, coated pits and lysosomes indicate a considerable degree of endo- or exocytosis in

SF.NSE ORGANS AND CENTRAL NERVOUS SYSTEM IN PARENTERODRILUS TAENIOIDES

123

Fig 2A-F. — I arenlerodrilus taen, aides. Sensory cells of palps. A. Collar receptors. B. Cilium and microvilli of collar receptor

in cross section. C. Multicihary sensory cell; nucleus (n) situated laterally. D. Cross section of apex of inulticiliary sensory

cell (sc); note clear vesicles accumulating in sensory cell. E. Group of sensory cells with intracuticular cilia; cross

sectioned cilia belong to ciliated epidermal cell; inset: sensory cilia in cross section. E. Presumed ocellus with phaosome

(ph). The arrow points to a sensory cell with intracuticular cilium. - cu cuticle, ep epidermal cell, m mitochondrion mv

microvillus, n nucleus, pc palp canal, ph phaosome. /rootlet, sc sensory cell, za zonula adhaerens.

Source

124

G. PURSCHKE & C. JOUIN-TOULMOND

these eells (Fig. 3A-B). Each sensory cell bears one cilium with a 9x2+0 axoneme and a few microvilli (Fig. 3A,

D). The ciliary rootlets are vestigial: 0.5 jam long and 0.04 pm thick. The ciliary shafts branch. In the branches the

microtubules are successively lost, resulting in structures indistinguishable from regular microvilli (Fig. 3D),

Microvilli and ciliary branches extend into die subcuticular space above die supportive cells outside die olfactory

chamber (Fig. 3A).

Presumed Ocelli. In each palp four presumed ocelli (type 1) have been found close to die main palp nerve

(Fig. 4). They consist of a single sensory cell characterized by an intracellular vacuole (phaosome) containing

numerous microvillus-like ciliary branches (Fig. 2F). There are no pigmented or unpigmented ocelli in the

prostomium of P. laenioides. However, die type-2 and type-3 unpigmented ocelli are located in the peristomium

(= head segment) in the lateral posterior ganglionic expansions of die brain (Figs 3E-F, 4). Each ocellus consists

of a sensory cell and a supporting cell forming an extracellular cavity. These cavities are completely filled with

microvillus-like branches of two cilia in bodi types. There are two of the minute type-2 ocelli (3x2x2 pm; Fig. 3E)

but five of the type-3 ocelli (18x6x4 pm; Fig. 3F) in each specimen investigated. Odier differences concern

position, branching pattern of cilia and arrangement of microvilli. The ocelli will be described in more detail

separately (Purschke & Jouin-Toulmond, 1993).

Central nervous system. The neuropile of the brain is situated in the prostomium in the curve formed by the

palp canals (Fig. 4). Conspicuous features are two pairs of dorsal expansions ( pe in Fig. 4) formed by nerve cell

processes and, posteriorly, by the perikarya of neurons and glial cells. These expansions extend far into the head

segment; the lateral ones contain the presumed ocelli. The ventral nerve cord communicates with the brain

through die circumoesophageal connectives (cc). Anteriorly, before Uiese nerves turn towards die brain, each

connective divides into a ventral (vrcc) and a dorsal root (drcc). The dorsal roots ( drcc ) and die nerve cell

processes of die lateral expansions (pe) enter the neuropile togedicr as one nerve. The nuchal nerve (nn) very

likely emanates from the lateral expansion (pe), whereas die medial expansion gives rise to a posteriorly running

dorsal nerve ( dn ). Although gut and stomodaeum are residual, die stomatogastric nerves are well-developed and

arise ventrally close to die ventral roots of the circumoesophageal connectives (vrcc). The main palp nerve (vpn4)

emanates laterally Irom die anterior part of die brain and receives its fibres from a dorsal and a ventral root. The

other palp nerves emerge directly from the roots of the circumoesophageal connectives: die second ventral palp

nerve ( vpn /) from die ventral root and die diin dorsal palp nerve (dpn) from die common nerve containing the

nerve fibres of the lateral posterior expansion and the dorsal root close to die brain.

DISCUSSION

The sense organs and the central nervous system of P. taenioides are structurally complex. Although the

digestive system is vestigial and not functioning (JOUIN, 1979, 1992), there is no evidence for a reduction of (he

sensory organs compared with other species ol the Protodrilida. However, do dicse organs provide additional

leatures to elucidate die phylogenetic relationship between them? In a phylogenetic tree previously suggested by

PURSCHKE & JOUIN (1988), Protodrilus and Parenterodrilus were sister groups forming die Protodrilidae which

is in turn the adelphotaxon ot Saccocirrus. Finally, these taxa most likely represent the sister group of

Protodriloides. Very likely, the taxon Protodrilida is related to the Spionida or one of its subordinate taxa

(ORRHAGE, 1974; PURSCHKE & JouiN, 1988; PURSCHKE, 1993). At present the Protodrilida is still retained

because its sistergroup has not yet been recognized.

I lie palps of P. taenioides are equipped widi a variety of sensory cells which allow reception of different

sensory stimuli from a wide area around die anterior end. They differ externally from those of Saccocirrus and

most Protodrilus species (except P. brevis-, see JOUIN, 1970) in die presence of modle cilia (Purschke, 1993). In

the Spionida such a filiation is generally present, located in a groove and used for collecting food particles

(Dauer, 1987; Fauchald & Jumars, 1979). Since a moudi is absent in P. taenioides, the remaining functions

10 -A.' - Parenterodrilus taenioides. A-D. Nuchal organ. A. Low power micrograph showing entire organ in cross

secuon: arrows point to sensory cell cilia; subcuticular space with microvilli Unv) and ciliary branches of sensory cells. B.

Ciliated cells with cover of microvillar tips (mvc). C. Microvillar tips in transverse section. D. Sensory dendrites with cilia

... and microvilli. E-F. Presumed ocelli. E. Small ocellus (type 2). F. Large ocellus (type 3); arrow points to sensory cell

dl'urn. - c cilium. cce ciliated supporting cell, coc coelcnchyme cell, cu cuticle, gc glial cell, in mitochondrion, mv

microvillus, mvb microvillus-like ciliary branch, mvc microvillar cover, och olfactory chamber, pe posterior expansion of

brain, r rootlet, nn reUactor muscle, si: sensory cell, sd sensory dendrite, sue supporting cell, za zonula adhaerens.

Source :

SENSE ORGANS AND CENTRAL NERVOUS SYSTEM

IN PARENTERODRILUS TAENIOIDES

125

Source : MNHN. Paris

126

G. PURSCHKE & C. JOUIN-TOULMOND

may be orientation in the interstitial medium and a more rapid exchange of water at the surface o! the animal.

Since motile cilia are also present on die palps of Protodriloides, diis character might be a vestige of a more

developed ciliation which could be assumed for die last common stem species with the Spionida. The sensory

cells with cilia penetrating die cuticle or with non-penetrative cilia are of minor phylogenetic importance, because

similar cells have been found in the other Protodrilida and they are not different from sensory cells generally

present in annelids (Storch & Schlotzer-Schrehardt, 1988; Purschke, 1993). Among the sensory cells of

die palps only the phaosomous ocelli can be considered for phylogenetic considerations. Phaosomes - intracellular

cavities containing die presumed light-sensitive organelles - occur only occasionally in polychaetcs (Purschke &

Jouin-Toulmond, 1993,). They are found neidier in Saccocirrus nor in Protodriloides but arc present in die

palps of several Protodrilus species (Purschke, 1993; Jouin-Toulmond & Martin, unpubl. observ.). These

phaosomes are structurally identical with diose of P. taenioides and, therefore, most likely represent a

synapomorphy of Protodrilus and Parenterodrilus.

With respect to the internal structure, the palps are most similar to those of Protodrilus. They differ from those

of Saccocirrus in die absence of the ampullae, posterior expansions of die palp canals. However, die palp canals

are considerably thinner in P. taenioides. and die musculature outside die canal and die blood vascular system arc

reduced compared with Protodrilus and Saccocirrus (PURSCHKE, 1993). The occurrence of a cord of coelenchyme

cells outside the canal and the loss of the external lamina between diem and the epidermis arc unique for P.

taenioides. These features are very likely correlated with die absence of podocytes, which form part of the wall of

the palp caiuds in die prostomium of Protodrilus and Saccocirrus (Purschke, 1993). In diese genera die palp

canals probably serve as a hydroskeleton filled with movable coelenchyme cells, and the podocytes have been

regarded as the site where fluid is introduced into die canals from the blood. Since movable coelenchyme cells, or

a fluid-filled lumen, are absent in P. taenioides. stiffness of the palps is very likely achieved by the musculature of

the palp canals and the external coelenchyme tissue. Consequendy, podocytes appear to be redundant.

The nuchal organs of all Protodrilida investigated, including P. taenioides , are almost identical in structure and

consist of the same types of cells as usually found in polychaetes (PURSCHKE, 1986, 1990a; Storch &

SchlOtzer-Schrehardt, 1988; RHODE, 1990). In nuchal organs which are not located in deep pits, the ciliated

suppordng cells generally show structural specialisations which cover and protect the cilia and microvilli of die

sensory cells. Paving-stone-like covers of microvillar endings joined by fine fibrils have only been found in the

Spionidae Pvgospio elegans and Scolelepis squamata (SCHLOTZER-SCHREHARDT 1987; RHODE, 1990) and in

every species of the Protodrilida, which indicates a high probability of synapomorphy of diis character.

The sense organs found in the posterior expansions of the brain in P. taenioides show striking similarities to

photoreceptors - for example, a great expanse of plasmalemma in die form of microvillus-like cell processes, and

the position of die organs beneadi the epidermis (Eakin & Hermans, 1988). Such presumed ocelli without

shading pigment have repeatedly been reported for polychaetes and many species possess at least one type of

these ocelli, often in addition to pigmented ones (PURSCHKE, 1992). Their great structural diversity, however,

makes it likely dial unpigmented ocelli evolved convergently several times in annelids. Unpigmented ocelli are

also present in every species of die Protodrilida. Apart from the ocelli (type 1) of the palps, die type-2 and type-3

ocelli of P. taenioides are completely different to any ocellus of Protodrilus. Due to their different position and

structure, die ocelli of P. taenioides are not homologous to the so-called statocysts, to die phaosomes or to die

pigmented eyes occurring in the prostomium of various Protodrilus species (Eakin el al.. 1977; PURSCHKE,

1990b,c). There are also no similarities to the presumed ocelli of Protodriloides (unpubl. observ.). On die odier

hand, there is a certain probability of homology widi die type-1 ocelli of Saccocirrus (PURSCHKE & JOUIN-

Toulmond, 1993). Since die sister group relationship between Parenterodrilus and Protodrilus is well

established by several synapomorphies, diis character may be regarded as a symplesiomorphy taken from die stem

species of saccocirrids and protodrilids.

The structure of die central nervous system and die innervation of die anterior end have great potential in

phylogenetic reconstruction (Orrhage, 1990, 1991). As shown previously, the brain with its nerves and the palp

anatomy of Protodriloides, Protodrilus and Saccocirrus give strong evidence for a relationship to the Spionida

(PURSCHKE, 1993). As was to be expected, the central nervous system of P. taenioides is very similar to dial of

Protodrilus and Saccocirrus and corroborates the general pattern observed; e.g., the roots of the

circumoesophageal connectives, the stomatogastric nerves and die palp nerves arise in corresponding positions,

die main palp nerve vpii4 has a ventral and a dorsal root, and the dorsal root of die circumoesophageal connectives

is much smaller than die ventral root. However, diere are only three palp nerves, which means, that die nerves

vpii2 and vpnj very likely have been lost; furdiermore, there is only one dorsal nerve and die posterior ganglionic

expansions of die brain are unknown in die other taxa. The nuchal nerve probably also has a different posidon.

SENSE ORGANS AND CENTRAL NERVOUS SYSTEM IN

PARENTERODRILUS TAENIOIDES

127

Shc°HREHALTfS7Tr^Spmay,haVe differ?"1 p,,si,ions in ,hc Spionkla as well (Orrhage, 1964 Schi otzer-

Z 1 ,US ,aemo,des- Neuropile of Ore brain (b) and associated nerves. Dorsal view on the left side the dorsal

PZ\°l 'he uC "erV0US SyJS,Cm has been omitted' reconstruction from electron microscopic ^observations cr

orean Pha§eal conn,cc,,ve- fn dorsal nerve. dpn dorsal palp nerve, drcc dorsal root of cr. nn nuchal nerve no nuchal

~ion/ofd^eScUmri T' '• 'ypC‘2 and ty'^-3 ocelli; och olfact°ry chamber, pc palp canal, pe ^sterm? gangTonk

expansion o t brain, sn stomatogastnc nerve, vp/iy 4 ventral palp nerve 1 ,4, vrcc ventral root of cc. g g

,'llC prcsent,tindinl8.s on P- laenioides corroborate its presumed relationship witli die other

the mnn tnt nf f0UP T '"T P 10 Pro'odrilus can be sustained by newly found synapomorphies: loss of

palp canals and presence of tentacular phaosomes. Several additional autapomorphtes clearly

' j *e derived position of P. taemoides : e.g„ coelenchyme cells present outside the palp canal loss of

podocytes in die canal, brain wttii posterior ganglionic expansions, loss of die palp nerves vpn2 and vpnj and loss

^^S^So^CharaCterS ^ l° bC PleSi°m0rphieS ^ 3 bellcr -'derstanding of the

128

G. PURSCHKE & C. JOUIN-TOULMOND

REFERENCES

DAUER, D.M.. 1987. — Systematic significance of the morphology of spionid palps. Bull Biol Soc. Wash., 7 : 41-45.

Eakin, R.M.. Martin. G.G. & Reed, C.T., 1977. — Evolutionary significance of fine structure of archiannelid eyes.

Zoomorphologie, 88 : 1-18.

Eakin, R.M. & Hermans, C.O., 1988. — Eyes. In: W. Westheide & C.O. Hermans (eds). The ultrastructure of Polychaeta.

Microfauna Mar.. 4 : 135-156.

FAUCHALD, K. & JUMARS, P.A.. 1979. — The diet of worms: a study of polychaete feeding guilds. Oceanogr. Mar. Biol. Ann.

Rev.. 17 : 193-284.

JouiN, C., 1970. Recherches sur les Protodrilidae (Archiannelides) : I. Etude morphologique et systematique du genre

Protodrilus. Cah. Biol, mar., 11 : 367-434.

JOUIN. C., 1979. — Description of a free-living polychaete without a gut: Asiomus laenioides n. gen., n. sp. (Protodrilidae,

Archiannelida). Can. J. Zool. , 57 : 2448-2456.

JouiN, C.. 1992. — The ultrastructure of a gutless annelid Parenlerodrilus gen. nov. laenioides (= Asiomus laenioides)

(Polychaeta. Protodrilidae). Can. J. Zool, 70 : 1833-1848.

ORRHAGE, L.. 1964. — Anatomische und morphologische Studien iiber die Polychaetenfamilien Spionidae. Disomidae und

Poecilochaetidae. Zool Bidr. Uppsala. 36 : 335-405.

ORRHAGE, L.. 1974. Ubcr die Anatomic, Histologic und Verwandtschaft der Apistobranchidae (Polychaeta. Sedentaria)

nebst Bemerkungen liber die systematische Stellung der Archianneliden. Z. Morph. Tiere, 19 : 1-45.

ORRHAGE. L., 1990. — On the microanatomy of the supraoesophageal ganglion of some amphinomids (Polychaeta. Errantia)

with further discussion of the innervation and homologues of the polychaete palps. Acta Zool. (Stockh.), 71 : 45-59.

ORRHAGE, E., 1991 . On the innervation and homologues of the cephalic appendages of the Aphroditacea (Polychaeta). Acia

Zool (Stockh.). 72:233-246.

PURSCHKE, G., 1986. — Ultrastruclure of the nuchal organ in the interstitial polychaete Stygocapitella subterranea

(Parergodrilidae). Zool Scr., 15 : 13-20.

PURSCHKE, G.. 1990a. — Comparative electron microscopic investigation of the nuchal organs in Protodriloides , Protodrilus

and Saccocirrus (Annelida, Polychaeta). Can. J. Zool, 68 : 325-338.

PURSCHKE, G., 1990b. — Fine structure of the so-called statocysts in Protodrilus adhaerens (Protodrilidae, Polychaeta). Zool.

Anz.. 224 : 286-296.

PURSCHKE. G., 1990c. — Ultrastructure of the "statocysts" in Protodrilus species (Polychaeta): reconstruction of the cellular

organization with morphometric data from receptor cells. Zoomorphology, 110 : 91-104.

PURSCHKE. G.. 1992. — Ultraslructural investigations of presumed photoreceptive organs in two Saccocirrus species

(Polychaeta. Saccocirridae). J. Morphol., 21 1 : 7-21.

PURSCHKE, G.. 1993. — Structure of the prostomial appendages and the central nervous system in the Protodrilida

(Polychaeta). Zoo morphology, 113 : 1-26.

PURSCHKE, G. & JouiN, C., 1988. — Anatomy and ultrastructure of the ventral pharyngeal organs of Saccocirrus

(Saccocirridae) and Protodriloides (Protodriloidae fam. n.) with remarks on the phylogenetic relationship within the

Protodrilida (Annelida: Polychaeta). J. Zool (Lond.), 215 : 405-432.

PURSCHKE, G. & JOUIN-TOULMOND, C., 1993. — Ultras tructure of presumed ocelli in Parenlerodrilus tcienioides (Polychaeta.

Protodrilidae) and their phylogenetic significance. Acta Zool (Stockh.), 74 : 247-256..

Rhode, B., 1990. Ultrastructure of nuchal organs in some marine polychaetes. J. Mo/phol, 206 : 95-107.

Sen lawny , A.. GRtJNIG, C. & PFANNENSTIEL, II. -Dm 1991. — Sensory and secretory cells of Ophryotrocha puerilis

(Polychaeta). Zoomorphology ,119: 209-215.

SchlOtzer-Schrehardt, U., 1987. — Ultrastructural investigations of the nuchal organs of Pygospio elegans (Polychaeta).

II. Adult nuchal organs and dorsal organs. Zoomorphology. 107 : 169-179.

Storch, v. & SchlOtzer-Schrehardt, U.. 1988. — Sensory structures. In: w. Westheide & C.O. Hermans (eds), The

ultrastructure of Polychaeta. Microfauna Mar.. 4 : 121-133.

Source : MNHN. Paris

14

Genome size in Polychaetes:

relationship with body length and life habit

R. SOLDI * L. RAMELLA * M. Cristina GAMBI **

Paolo SORDINO ** & Gabriella SELLA *

* Department of Animal Biology

University of Turin, via Accademia Albertina 17

10123 Torino, Italy

** Laboratorio di Ecologia del Benthos

Stazione Zoologica " Anthon Dohm"

80077 Ischia, Napoli, Italy.

ABSTRACT

Only a few species of polychaetes have previously been analyzed for nuclear DNA content (CONNER et al. .1972). by

means of microdensi tome trie analysis of the amount of Feulgen-stained DNA in interphase nuclei. We have correlated genome

sizes of 47 species of Polychaeta with mean body length of adult worms. In the species examined genome sizes ranged from

0.07 to 1.2 pg of DNA per nucleus in interstitial species and from 0.4 to 7.2 pg in macrobenthic species. The lowest values are

among the lowest genome sizes of invertebrates so far investigated. Genome size appeared to be significantly correlated with

mean body length (r = 0.30: df = 45; 0.05 < P < 0.01 ), which ranged from 0.9 mm to 250 mm in the species we examined.

RESUME

Taille du genome chez les Polychetes : rapports avec la taille du corps et Phabitat

Le contenu nucleaire en ADN chez les Polychetes a ete jusqu'a maintenant etudie chez ties peu d'cspeces (CONNER et al.,

1972). La taille du genome de 47 especes de Polychetes a ete mesuree a I’aide d'une analyse microdensitometnquc de la

quantite d’ADN dcs noyaux en repos colores par la reaction de Feulgen. Cette taille a ete correlee avec la longueur moyenne du

corps des annelides adultes do chaque espece. La quantite d'ADN haploide varie de 0.07 a 1,2 pg chez les especes de la

meiofaune et de 0,4 pg a 7.2 pg chez les especes macrobenthiques. Les valeurs les plus petites sont parmi les plus faibles

mesurees chez loutes les especes d’invertebres analysees jusqu'a maintenant. La longueur moyenne du corps des especes

examinees cst comprise entre 0,9 mm et 250 mm, et est significativement correlee avec la taille moyenne du genome (r = 0.30 ;

df = 45; 0.05 < P < 0.01 ), chez les especes etudiees.

INTRODUCTION

Genome size (also known as the C-value) is defined as the mass of DNA in a haploid genome (HlNEGARDNER,

Soldi. R., Ramella, L., GAMBI, M.C., SORDINO. P. & G. Sella. 1994. — Genome size in Polychaetes: relationship with

body length and life habit. In: J.-C. Dauvin. L. LAUBIER & D.J. REISH (Eds), Actes de la 4eme Conference internationale des

Polychetes. Mdm. Mus . natn. Hist, not., 162 : 129-135. Paris ISBN 2-85653-214-4.

Source MNHN. Paris

130

R. SOLDI. L. RAMELLA. M.C. GAMBI. P. SORDINO & G. SELLA

1976). Genome size is known to be positively correlated will) cell volume and size, length of cell cycle, duration

of meiosis and developmental rates (Cavalier-Smith, 1985; McKinney & McNamara, 1991). These

correlations are believed not to be a direct function of genome size but to result trom a balance between selective

forces favoring larger cells, and hence larger genomes, and those favoring rapid cell multiplication (more easily

achieved with small cells and small genome sizes).

Very small organisms, such as those in die interstitial marine fauna, have never been examined to test whedier

Uiese relationships apply. In addition to their small size, interstitial organisms have so many biological and

ecological adaptations to life in a harsh and variable environment, such as die sediment interstices, that they can

be considered very specialized living forms (WESTHEIDE, 1984).

Among lower invertebrates, polychaetes show die highest variety in body sizes and morphology; this reflects

their high diversity of niches and life histories. Their morphological variation is probably due to their plasticity

and early evolutionary radiation (Fauchald, 1984). Among polychaetes, nine families arc exclusively

represented by interstitial taxa (WESTHEIDE, 1985, 1990) and many others have intersdtial representatives (e.g.

Mesionidae, Syllidae, Dorvilleidae). These organisms dius could represent good "biological tools" for studying

relationships between genome size, body size and organizadon. Up to now data on genome size for the Polychaeta

are scarce. Only Conner et al. (1972) measured nuclear DNA amounts for several species of polychaetes by

means of microdensitometric determinations of Feulgcn dye content of somatic nuclei and fluorimetric

quantitation of the DNA of sperm cells. However, among the species considered by Conner et al. (1972). diere

were no interstitial taxa.

This report is a first attempt to test the hypothesis that, in polychaetes, a positive corrclauon between genome

size and Ixxly size may be expected, especially when intersdtial forms are included in the study.

MATERIALS AND METHODS

To die 27 species of polychaetes considered by Conner et al. (1972) we added 20 species. They were chosen

on the basis of their availability. Among the species considered, 13 belong to the meiofauna and 34 to die

macrofauna. Among the interstitial species, three belong to exclusively interstitial families (Saccocirrus

papillocercus, Mesonerilla intermedia, Dinophilus gyrociliatus).

Individuals of 0. labronica and 0. puerilis were collected in 1991 in the harbour of Genoa (Italy) and

individuals of D. gyrociliatus were collected in 1992 in die aquarium of Leghorn (Italy). Specimens of 0. robusta

and 0. macrovifera came from strains set up in 1988 with animals collected in die harbour of Genoa. Specimens

of 0. gracilis came from a strain set up with animals collected at the isle of Sylt (Germany) in 1987, specimens of

0. diadema came from a collection made in 1989 at Long Beach (U.S.A.), specimens of O. hartmanni came from

individuals collected in 1990 in Algeciras (Spain). Individuals of 0. I. pacifica were collected from Woods Hole

aquariums in 1984 and individuals of 0. costlowi from aquariums of Tampa (Florida) in 1986. 0. notoglandulata

individuals came from a 1979 collection in die Sagami Bay (Japan). All these strains of Opliryotrocha were

kindly provided to us by Prof. B. Akesson, Individuals of the odier species were collected in autumn 1990 and

spring 1991 in two coastal biotopes of die island of Ischia (Gulf of Naples, Italy).

The interstitial taxa as well as P. kefersteini and O. flexuosus (see Table 1) were collected in very coarse sands

located at around 8-10 m deptli mid characterized by a typical "Ampltioxus- sand" community (Picard, 1965). The

other macrofaunal species (S. prolifera. P. dttmerilii, A. mediterranea, S. Spallanzani and B. luctuosum ) were

collected in very shallow ( 1 -3 m depdi) hard bottoms covered by photophylic algae, mainly die brown macroalgae

Cystoseira crinita and Halopteris scoparia. To measure genome sizes, cellular suspensions of whole animals

were splashed on cool slides, subsequently air-dried and stained with the Feulgen reaction according to the

procedure of Itikawa & Oglra (1954). Evaluation of die Schiff-positive material was carried out widi a Vickers

M86 microdensitometer at a wavelength of 545 ± 5 inn. For absolute DNA calibration mouse sperm and

lymphocyte preparations were stained together with polychaete preparations. For each species several slide

preparations were obtained with 2 to 20 individuals, according to the availability of live material. At least 50

nuclei per species were measured from different slides (including both spermatozoa and spermatids, when

present) except for O. flexuosus mid M. intermedia where only 20 nuclei could be measured. The absorption

values obtained as arbitrary units were plotted as percent frequency distribution histograms in order to identify the

1C, 2C, 4C classes of DNA. When die DNA values of sperm were not available, the 1C class value was inferred

by halving the 2C class. For die evaluation of absolute DNA amounts, values obtained as arbitrary units were

Source :

GENOME SIZE. BODY LENGTH AND LIFE HABIT IN POLYCHAETES

131

'Fable 1. — Range and mean of body length (mm) and haploid nuclear DNA content (in pg) by microdensito-

metric and fluorimetric determination in 47 species of polychaetes. Fluorimctric data are indicated without

standard error. * = meiofaunal species; a = present paper; b = Conner et ai (1972).

132

R. SOLDI. L. RAMELLA, M.C. GAMBI. P. SORDINO & G. SELLA

Tabi E 1 (continuation) - Range and mean of body length (mm) and haploid nuclear DNA content (in pg) by

SSI nuorimetric determination in 47 species of Seated

without standard error. * = mciofaunal species; a = present paper; b = CONNER el al. ( 1 )72).

0 O. obscurus, reported as Podarke obscura in Conner el al. (1972)

° L. ambigua , reported as Pseudeurythoe ambigua in Conner el al. (1972)

° /\. inagna . reported as Onuphis magna in Conner el al. (1972)

* O. labronica pacifica , not yet formally described, Akesson (1984)

** O. robusta and inacrovifcra , not yet formally described. Akesson (1975)

0 L fragilis, reported as Scoloplos fragilis in Conner el al. (1972)

0 C. grandis, reported as Cirralulus grandis in Conner el al. (1972)

0 A. mucosa . reported as Clymenella mucosa in Conner et al. (1972)

0 R. crisp urn, reported as Branchiomma nigromaculaia in Conner el al. (1972)

Source :

GENOME SIZE, BODY LENGTH AND LIFE HABIT IN POLYCHAETES

133

converted into picograms, taking die mouse genome size as 3.9 picograms (Sparrow et al. , 1972). To calculate

the correlation between genome size and organism size, we considered body length as an estimate of body size.

We arc aware that in polychaetes body length is a simplistic measure of body size, and that not always is this

parameter positively correlated with the actual size of the worm (DUCH&NE, 1982). Besides, body length can

greatly change in different populations of the same species according to geographic location (climatic), local

environment and trophic conditions, and laboratory conditions in the case of laboratory reared populations. High

body length variability in polychaetes notwithstanding, in order to compare our data with those of Conner# al .

(1972), we used the body length variable because it was the only size-parameter available from the literature. An

indicative mean body length for each of the species considered was estimated by comparing and averaging body

length data given by different authors. In Table 1 we reported the range of adult body length values, as well as a

mean value obtained by averaging values obtained from literature. For the species in our study, we integrated the

literature data with the values obtained by measuring at least 10 adult individuals from sampled populations. For

the gonochoric species of the genus Ophryotrocha 10 sexually mature males and mature females were considered.

In D. gyrociliatus only females were measured, in simultaneously hermaphroditic species only sexually mature

individuals and in protandric sequential hermaphroditic species, worms were measured when they reached the

female phase.

This approach allowed us to assess at least the actual "order of magnitude" of body length reached within each

single species.

RESULTS AND DISCUSSION

Genome sizes expressed as pg of DNA per haploid nucleus and mean body lengths of the species examined by

us and by CONNER et al. (1972) arc listed in Table 1, ranking them by orders and families according to PETTIBONE

classification (1982). A total of 47 genome sizes are listed, 10 of which were measured by Conner et al. (1972)

with the fluorimetric method. The species examined belong to 23 families and 12 orders and are therefore

representative of a broad evolutionary range within die class and of a wide spectrum of life habits, mainly

represented by shallow- water species.

Genome sizes varied among species from 0.07 pg to 7.2 pg DNA per nucleus. Such a 100-fold range in

genome size is comparable only to die ranges found in insects and teleosts. All other animal classes are much

more conservative in their genome sizes (JOHN & MlKLOS, 1987). Some of the genome sizes observed in

polychaetes are among the lowest found in invertebrates so far investigated. Only Eutardigrada (REDI &

Garagna, 1987) and some nematodes (John & MlKLOS, 1987) have the same or smaller amounts of DNA.

Genome size appealed to be significantly positively correlated with body length (r = 0.30; df = 45;

0.05 < P < 0.01). However, only 9 % (i.e. r2) of the variation in genome size is explained by its relationship to

body length. In die 13 interstitial species included in the sample (Ophryotrocha spp., S. papillocercus , D.

gyrociliatus, M. intermedia ) no significant correlation was observed between genome size and body length, but by

their small body size and small genome size, diey greatly contributed to the significance of die overall r. If they

were excluded, die correlation was no longer significant.

Different and contrasting patterns arise in comparing from an evolutionary view point die DNA content in

polychaetes. At the generic level, die 10 species of Ophryotrocha showed quite homogeneous values, except O.

hartmanni , as discussed by Sella et al. (1993). Furdiermore, P. kefersteini , that, like Ophryotrocha , belongs to

die Dorvilleidae family, showed a comparable value. On the other hand, die Uiree species of the genus Cirriformia

showed quite different DNA amounts (Table 1). At the family level, die Sabellidae (5 species) demonstrated a

high variability in genome size, while the Onuphidae (3 species) and the Polynoidae (2 species) showed more

homogeneous values. The species belonging to exclusively intersutial families (D. gyrociliatus , M. intermedia and

S. papillocercus) have among die smallest DNA amounts. At the order level, one may note that within die

Eunicida, die macrofaunal taxa (Onuphidae, Lumbrineridae) have higher DNA amount than the interstitial ones

(Dorvilleidae) (Table 1).

Although the sample of interstitial polychaetes is still quite small, diese first results suggest that mciofaunal

taxa have on the whole smaller genome sizes than macrofaunal ones.

We speculate diat the small genome sizes characteristic of mciofaunal species may be partially correlated, not

only with body size (not all the interstitial species have necessarily very small dimensions, e.g. S. papillocercus)

but also widi those biological features deriving from an intersutial life habit, such as progenesis (i.e. retention ot

134

R. SOLDI. L. RAMHLLA. M.C. GAMBL P- SORDINO & G. SELLA

juvenile characters produced by a genetically fixed precocious sexual maturation (Gould. 1977), short life-span,

rapid sexual maturation, rapid cycling of generations, few eggs of large size, and brooding.

These features, which are well documented in Opliryotroclia spp., Dinophilus spp. and in many other

meiofaunal polychaetes (SWEDMARK, 1964; WESTHEIDE, 1984), make up life histories with peculiar mosaics of

V and "K" selected parameters. One may also speculate that small genome sizes can be a prerequisite to

interstitial life.

The above considerations are still quite speculative due to the small amount of data to date available on tins

subject; further analyses on genome sizes in other species of macrofaunal and meiofaunal polychaetes are

necessary to corroborate the hypothesis dial interstitial polychaetes have smaller genomes than macrofaunal

polychaetes. On the whole, the DNA content in polychaetes showed a wide range of values and a large variability.

Such features are common to many other biological properties of this highly diversified group of marine

organisms.

ACKNOWLEDGEMENTS

This research was in part supported by a grant from the Italian M.U.R.S.T. (Progetto Genetica

Evoluzionistica). We thank Hie Centro di Studi per 1'Istochimica of die C.N.R. (Pavia) for kindly allowing us to

use their instruments and Paola Protto for her technical assistance.

REFERENCES

Akesson. B. 1975. — Reproduction in the genus Opliryotroclia (Polychaeta, Dorvilleidae). Pubbl. Staz. zool. Napoli. 39

Suppl. : 377-398.

AkessON. B.. 1984. — Speciation in the genus Opliryotroclia (Polychaeta, Dorvilleidae). In: A. FISCHER & H.D.

Pfannenstiel (eds), Polychaete Reproduction. Fortschr. Zool. : 299-316.

Cavalier-Smtih. T.. 1985. — The Evolution of Genome Size. John Wiley & Sons. Chichester. NewYork. Brisbane. Toronto.

Singapore, 523 pp.

CONNER. W. G., HlNEGARDNER, R. & Bachmann. K., 1972. - Nuclear DNA amounts in Polychaete Annelids. Experientia ,

28 : 1502-1504.

DUCHfcNE, J.C.. 1982. Problemes lies a la croissance chez les Annelidcs Polychetes. Ocean is, 3 : 493-504.

FauchalD, K., 1984. — Polychaete distribution pattern, or: can animals with Palaeozoic cousins show large-scale

geographical patterns ? In: P.A. HUTCHINGS (ed.), Proc. First International Polychaete Conference, Linnean Society of

New South Wales: 1-6.

Gould. S.J.. 1977. — Ontogeny and Phytogeny. Belknap Press of Harvard University Press, Cambridge Massachusetts and

London U.K.. 501 pp.

HlNEGARDNER, R., 1976. — Evolution of genome size. In: Ayala (ed.). Molecular Evolution. Sinauer Assoc. Inc. Sunderland.

Massachusetts : 179-199.

Itikawa, O. & Ogura. Y., 1954. — The Feulgcn reaction after hydrolysis at room temperature. Stain Technology. 29: 13-15.

JOHN, B.& Miklos. G.L.G.. 1987. The Eukaryote Genome in Development and Evolution. Allen and Unwin, London. 291

pp.

McKinney, M.L. & McNamara, K.J.. 1991. Heterochrony. The Evolution of Ontogeny. Plenum Press, New York and

London. 437 pp.

PETTIBONE, M.. 1982. — Annelida. In: S.P. PARKER (ed.). Synopsis and Classification of Living Organisms. McGraw Hill,

London : 43 pp.

Picard, J.. 1965. Recherches qualitatives sur les biocenoses marines des substrats meubles dragables de la region

marseillaise. These. Fac. Sc. Nat. University d’Aix-Marseille, 160 pp.

REDI. C.A. & GaraGNA, S., 1987. Cytochemica! evaluation of the nuclear DNA content as a tool for taxonomical studies in

Lutardigrades. In: R. BERTOLANI (ed.). Biology of Tardigrades. Selected Symposia and Monographs U.Z.I. Mucchi,

Modena, 1 : 73-80.

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GENOME SIZE. BODY LENGTH AND LITE HABIT IN POLYCHAETES

135

SELLA. G.. Redi. C.A.. RAMELLA. L.. Soldi. R.. Premoll M.C. — 1993. Genome size and karyotype length in some

interstitial polychaete species of the genus Ophryotrocha ( Dorvilleidae). Genome, 36 : 652-657.

Sparrow, ATI., Price, II.J. & UNDERBRINK, A.G.. 1972. — A survey of DNA content per cell and per chromosome of

prokaryotic and eukaryotic organisms: some evolutionary considerations. In: J. Smith (ed.). Evolution of genetic systems,

Brookhaven Symposia in Biology., 23. Gordon and Breach. New York: 451-494.

SWEDMARK, B.. 1964. — The interstitial fauna of marine sand. Biol. Rev., 39 : 1-42.

WESTHEIDE, W., 1984. — The concept of reproduction in Polychaetes with small body size: adaptations in interstitial species.

In: A. FISCHER & H. D. PFANNENSTIEL (eds), Polychaete reproduction. Fortschr. Zool. , 29 : 265-287.

WESTHEIDE, W.. 1985. — The systematic position of the Dinophiliidae and the Archiannelid problem. In: S. Conway

MORRIS, D. George. R. Gibson & H.M. Platt (eds), The origin and relationships of lower invertebrates. Oxford

University Press. Oxford : 310-326.

WESTHEIDE, W., 1990. — Polychaetes: interstitial families. Synop. Brit. Fauna, 44 : 1-153..

Source : MNHN. Paris

15

Fine morphology of the feeding apparatus of

Cossura sp. (Polychaeta, Cossuridae)

from the White Sea

Alexander B. TZETLIN

Dept, of Invertebrate Zoology

Moscow State University

Moscow, Russia

ABSTRACT

Morphology of the feeding structures and construction of the anterior part of the body cavity of Cossura sp. from the

While Sea were studied using TEM and SEM techniques. Buccal tentacles are the only feeding structures in the spacious

buccal cavity. They are situated on the dorsal surface of the buccal cavity near the esophageal opening. There are about 15

buccal tentacles covered by long cilia inside the proboscideal cavity. In cross sections every tentacle consists of

columnar epithelial ciliated cells and in the central part, inside a ring of basal membrane, there arc two longitudinal

muscle cells and two cells without contractile filaments. The space between body wall and tissues of digestive tract is

occupied by the non-contractile cytoplasmic parts of longitudinal muscle cells of the body wall. Buccal tentacles cannot

be protracted by hydrostaic pressure of the body cavity, as there is no free coelom ic space either in the anterior part of the

body or inside the tentacles. Also Cossura sp. has not circular muscles in the body wall which are usually necessary for

hydrostatic skeleton. It seems that natural position for the buccal tentacles during feeding processes is partly projected

from the very widely open mouth. According to our observations on living specimens, the long unpaired dorsal branchial

filament never takes part in feeding, it is always stretched along the trunk, and has presumably a respiratory function.

RESUME

Morphologie fine de I'appareil alimentaire de Cossura sp. (Polychete, Cossuridae) de la mer

B 1 a n c h e

La morphologic des structures trophiques ct la constitution de la parlie anterieure cavitairc du corps de Cossura sp. de

la mer Blanche ont etc (Studiees en utilisant les techniques de miscroscopie electronique a transmission et de microscopie

electronique a balayage. Les tentacules buccaux sont les seules structures servant a l'alimentation, presentes dans la vaste

cavite buccale. II y a environ 15 tentacules couverts de longs cils a l'interieur de la cavite proboscideale. En coupe, chaque

tentacule esl constitue par des cellules epitheliales cilices en forme de colonnes et dans la partie centrale. a l'interieur d’un

anneau de la membrane basale, il y a deux cellules musculaires longitudinales et deux cellules sans filaments contractiles.

L'espace entre la paroi du corps et les tissus du tractus digestif est occupe par les parties cytoplasmiques non contractiles

des cellules musculaires longitudinales de la paroi du corps. Les tentacules buccaux ne peuvent etre developpes par la

pression hydrostatique de la cavite corporelle, tout comme il n'y a pas d'espace coelomiquc libre ni dans la partie

Tzetlin, A.B., 1994. - Fine morphology of the feeding apparatus of Cossura sp. (Polychaeta, Cossuridae) from the

White Sea. In: J.-C. Dauvin. L. LaUBIER & D.J. REISH (Eds), Actes de la 4eme Conference internationale des Polychetes.

Mem. Mus. natn. Hist, nat ., 162: 137-143. Paris ISBN 2-85653-214-4.

Source : MNHN. Paris

138

A. R. TZBTLIN

anicrieurc du corps ni clans les lentacules. De meme. Cossura sp. n'a pas dc muscles circulaires dans la paroi du corps,

lesquels sont habituellemenl necessaires pour le squelettc hydrostatique. En position naturelle durant les phases

d'alimentation. les tentacules buccaux semblent Stic partiellement projetiSs hors de la bouche ties largement ouverte.

Suivant nos observations sur des animaux vivants. le long filament branchial dorsal ne joue aucun role dans

l'alimentation. II est toujours accole le long du tronc et a. probablement. unc fonction respiratoire.

INTRODUCTION

The Cossuridae is one of die most poorly studied polychaete families. We have very nearly no information

even about die general anatomy of Uiese worms. In addition there is almost no information about life style and

feeding in diese°animals (Fauchald & Jumars, 1979; Fournier & Petersen, 1991). Thulin (1921) and later

Fournier & Petersen (1991) described die ciliated "buccal tentacles" of die pharyngeal cavity of Cossura as die

feeding apparatus of these polychaetes. Up to this time die construction, position in the pharyngeal cavity and

functioning of die cossurid mouth parts have remained unknown.

This paper deals widi die fine morphology of the feeding structures and die construction of die anterior part of

die body cavity of Cossura sp. from die White Sea.

MATERIALS AND METHODS

All material (about 100 specimens) was collected within 20 km of Velikaya Salma Straight (Kandalaksha Bay,

the White Sea. 66° 30'N, 33° 30'E), in die depdis varying from 20 to 30 m by means of SCUBA.

The While Sea Cossura sp. inhabits die upper layer (1-2 cm) of muddy sediment in depdis of more dian 20 m.

Previously, this species was identified as Cossura longocirrata Webster & Benedict (Tzetlin,1981), but according

to Petersen (personal communication) die White Sea animals must be referred to anodier, possibly new species.

Live worms were examined in the Laboratory of die White Sea Biological Station of Moscow University. Hie

observations on die Cossura sp. were made in a small aquarium widi a 3 cm sediment layer transferred Irom the

depth of 25 m.

Animals were fixed widi 2,5 % glutaraldehyde, buffered with 0,2 M Na-cacodylate buffer (pH = 7,2-7.4) with

the addition of 0,131 g sucrose per 1 ml of solution (1 hour) and postfixed with 1 % osmiumtelroxide solution in

the same buffer. For SEM observations specimens were critical-point dried after dehydration in an elhanol series

and widi acetone and dien after coating widi gold. They were studied widi a Hitachi S 405 microscope. For TEM

fixed specimens were dehydrated in an ethanol series, treated widi acetone and embedded in Epon. Semidiin sections

were made with glass knifes on a Dupont Ultracut microtome and stained in 1 % toluidine blue. Ultradiin sections

for TEM observations were cut on a LKB-3 Ultracut microtome widi diamond knife, stained in lead citrate and

uranylacetate and then examined with a JEM-lOOb microscope. More dian 50 specimens were studied by light

microscopy in living condition, 25 specimens were observed with SEM. Fifteen of diem were cut in the sagittal

plane by microsurgery knife and the dissected worms examined widi SEM. Four specimens (two sagittal and two

transverse series) were examined with TEM techniques.

RESULTS

Construction of the feeding apparatus. — Cossura sp. are slender polychaetes of 20-30 mm length, with

50-60 setigers. The T-shaped moudi opening is located in die fissure between two secondary "segments" of the

peristomium. The only external appendage on the anterior part of die body is die dorsal branchial filament, which

originates from die border between the second and third setigers. The branchial filament bears a longitudinal row of

cilia. The inner part of die branchial filament contains longitudinal muscle cells, and two blood vessels. There is

also a narrow coelomic space.

The spacious buccal cavity stretches from the anterior border of peristomium to the border between setigers 2

and 3. In the last area is also die junction between foregut and intestine. The exdemely short esophagus is

represented by short funnel widi relatively narrow lumen between stoinodeum and intestine (Fig. 1 A).

Slomodeal epithelium consists of squamous (1,6 pm) cells rarely covered by short microvilli (Fig. 1B-C; Fig.

3. C-D). A collagenous matrix on die surface of the slomodeal epidielium is poorly developed. There are electron

dense secretory spherulae (D =0,5-0,4 pm) in the epidielial cells. The epidielium is underlain by a thin basal

MORPHOLOGY OF FEEDING APPARATUS OF COSSURA SP.

139

lamina (0,4 |im) and peritoneal cells. The wall of buccal cavity lacks muscle cells (Fig. 1, B-C; Fig. 3, C-D).

Epithelial cells in the back region of the stomodeum are covered with cilia (Fig. 1, A, B). These cells are similar

to epithelial cells of the esophageal region and anterior part of intestine.

A b

FIG. 1. — Cossura sp. A. : scheme of sagittal section. Arrows B, C show position of transverse sections. B, C -

transverse sections through the region of the foregut (hemischeme, after TEM -reconstructions). Scale: A - 0.5 mm, B, C

- 0,1 mm. be: buccal cavity, bf: branchial filament, bbf: blood vessel of the branchial filament, bte: buccal tentacle, bz:

basal zone of the buccal tentacle, c: cilia, ch: chaeta. elm: cytoplasmic expansion of the longitudinal muscle cell, coc:

coelomic cavity, dbv: dorsal blood vessel, ep: epitermal epithelium, in: intestine. 1m: longitudinal muscle cell, mo:

mouth opening n: nucleus, nf: nerve filament, nlm: nucleus of- the longitudinal muscle cell, oe: oesophagus, omc: oblique

muscle cell, pco: parapodial complex, r: rootlets, step: stomodeal epithelium, sg: secretory granulae. tep: tentacular

epithelium, vbv: ventral blood vessel, vne: ventral nerve cord.

140

A. B. TZETLIN

Buccal tentacles, the only feeding structures, are located in the spacious buccal cavity. 1 hey are attached to the

dorsal surface of the buccal cavity near the opening into esophagus. There are about 15 buccal tentacles covered

with long cilia occupying almost all space inside the buccal cavity (Fig. I, A. B, C). The length of the buccal

tentacles is 0,6 - 0,7 mm and the widdi about 0,05 mm. The ventral and lateral surfaces of tentacles tire more

densely ciliated than the dorsal surface.

The ciliated epithelium of die buccal tentacles consists of high (20 pm) cells (Fig. 2). Basal bodies and

rootlets (with a length of about 18-20 pm) are well developed especially in the epithelial cells placed laterally on

the tentacles (Fig. 3. B). Ciliated cells have two types of secretory vesicles: electron dense spherulae (D= 0.5-

0,4 pm), the same as in the epithelial cell of the buccal wall. The other type of vesicles (D= 0,8 pm) is lull of

gray, non-structured serous-like matter. The epithelial cells have large nuclei (D= 5 pm).

r

c

Fig. 2. — Cossura sp.: Cross-section of the buccal tentacle (slightly schematic, after TEM-reconstruction). Scale:

0,025mm. For abbreviations, see Figure 1.

The epithelium of the buccal tentacles is underlain by basal lamina (0,16 pm) which rings die central zone.

There arc two groups of nerve fibres located laterally along die both sides ol die basal lamina cylinder.

Transverse sections show two longitudinal muscle cells and two supporting (or coelenchyme-like) cell widi

almost empty cytoplasm, within die ring of basal lamina. It is possible, that die last structures are only

cytoplasmic parts of die muscle cells. The coelomic cavity does not extend into die central cylinder of the tentacles

(Fig. 3, A).

Construction of body wall and coelomic lining of the anterior end of the trunk. — I here are

only longitudinal muscle cells in dirce bundles (two ventro-lateral and one unpaired dorsal longitudinal bundle)

under die ectodermal epidielium mid basal lamina. Circular muscles are very poorly developed and could be seen

only in die areas of inter-segmental fissures. Oblique muscles are located in die region of die parapodial

complexes. All longitudinal muscle cells have a spacious non-contractile cytoplasmic expansion in which the

nucleus is found. These cytoplasmic extension occupy all die space of the body cavity in the anterior setigers and

fit closely to die peritoneal cells which surrounds the foregut (Fig. 3, C). The little space free of cell bodies is

Source :

MORPHOLOGY OF FEEDING APPARATUS OF COSSURA SP.

141

only in the dorsal region of the third setiger. It is directly connected to the coelomic cavity of the branchial

filament.

FIG. 3. Cossura sp.: A. Central part of buccal tentacle in transverse section (TEM); B, ciliated epithelial cell of the

buccal tentacle (TEM); C, part of a transverse section through anterior part of the body (TEM); D. part of the

epithelium of the middle part of the buccal cavity (TEM). Scale: A. 0.003 mm, B, C, 0.014 mm. D. 0.0045 mm.

For abbreviations, see Figure 1.

Living observation. — The worms do not build massive tubes, but continuously produce mucus which is

always covered with sediment particles. The long dorsal branchial filament never takes part in feeding, being

always stretched along the trunk inside the mucous tube presumably having only a respiratory function. After

extraction from the sediment the worms usually break up into fragments and die rapidly.

142

A. B. IZETLIN

Buccal tentacles are normally located inside the buccal cavity. Only few worms with buccal tentacles extended

from die mouth were observed. The tentacles were motionless and non-contractile. All these animals were in bad

condition and convulsively contracted the anterior end. These worms were unable to retract their buccal tentacles.

FIG 4. Co ssura sp.: Hypothetical

position of Co ssura sp. during feeding processes. For abbreviations, see Figure 1.

DISCUSSION

The central cylinder of die buccal tentacles of Cossura consists of longitudinal muscle elements and supporting

(coelcnchyme-like) elements. A small coelomic space free from the cell bodies in die dorsal region of die third

setiger was found (between die branchial filament and the base of die buccal tentacles), but no coelomic space is

present in the buccal tentacles. It is theoretically possible dial powerful contractions of the longitudinal body

muscles, coupled widi a contraction of the branchial filament could cause die extrusion of die buccal apparatus. In

a great number of polychaetes, extrusion of tentacular or palpal structures when hydrostatic pressure is used, is

strongly correlated with the presence of special compartments of die coelom with muscular walls (ampullae of

Spionida, Protodrilidae and Saccocirridae and diaphragms in die Terebcllida).

Thus, it is unlikely that contraction of the longitudinal body muscles, coupled with a contraction of die

branchial filament may be die normal mechanism of tentacle elongation. It is more probable dial die supporting

elements of the central cylinder of die buccal tentacles form a kind of chord, supporting the constant shape mid

volume of the tentacle. Construction of the central cylinder of Cossura is similar to die construction of the palpal

canal of Protodriloides chaetifer (Purschke, 1993). In both cases there are longitudinal muscle elements (without

circular elements) and supporting (coelenchyme-like) elements. P. chaetifer and P. symbioticus differ from odier

Protodrilida (Protodrilidae and Saccocirridae) by die absence of ampullae and circular muscle in die wall of the

palpal canal. Although the diameter of the buccal tentacles of die Cossura is twice as large as diat of die palp of

Protodriloides, die number of longitudinal muscle cells in the central cylinder (two in a cross-section) is rather less

than in the palpal canal of Protodriloides (seven-eight, PURSCHKE, 1993). Considering dieir structure, the buccal

tentacles of Cossura must be little movable. So, die tentacles of Cossura are not able to move actively along die

surface of the substratum and the enormous elongations so typical for tentacles of the Terebellida (SUTTON, 1957).

Living observation (unfortunately very limited) also support diis conclusion. Protraction of die whole buccal

cavity as a component of normal feeding behavior (as suggested by Thulin. 1921 and Fournier & Petersen,

1991) is hardly probable since we did sec observe any system of retractors connected to the tentacles or the foregut.

The only possible hypothesis seems to be diat the buccal tentacles will be exposed to the substratum when the

mouth is opened very wide (Fig. 4). In this case tentacles may be pressed down onto the sediment. The high

density of cilia on die lateral and ventral surfaces of buccal tentacles supports this assumption. However, the

mechanism of contact of the feeding apparatus of Cossura widi sediment is not absolutely clear.

From a functional point of view the cossurid tentacular apparatus appears similar to the ciliated pharynx of

adult Orbiniidae (Fauchaed & JUMars, 1979). In morphological terms, die buccal tentacles of die Cossuridae

differ considerably from the tentacular apparatus of die Terebellida bodi in position and way of action. In the

ferebellidae and Alvinellidae tentacles are located on die outer surface of die upper lip, in die Pecunariidae on die

MORPI IOLOGY OF FEEDING APPARATUS OF COSSURA SP.

143

level of mouth opening, and in Ampharetidae liie tentacles are on the inner surface of the upper lip of the mouth

(Fauvel, 1897; Dales, 1962, DesbruyEres & Laubier, 1986). In contrast, the tentacles of die cossurids are

situated on the dorsal surface of buccal cavity near the esophageal opening. The hydrostatic mechanism of tentacle

elongation is associated with a special organ in the body cavity of Terbellida, in die form of a muscular diaphragm

widi paired reservoirs (Dales, 1962; Sutton, 1957). Such devices are absent in Cossuridae. The ciliated tentacles

of Cossuridae may be derived from ciliated structures on die dorso-Iatcral surfaces of buccal cavity common in a

number of different polychaete families (PURSCHKE, 1984, 1985, 1987; TZETLIN, 1991).

AC KN O W LEDGMHNTS

I am grateful to kindness of Mr. Michail Saponov and Drs. Oleg MALUTIN, Igor Kosevitch and Alexey

Elfimov for assistance in sampling. I am also grateful to Dr. Mary PETERSEN and Mrs. Marina Saphronova for

fruitful discussions and Drs Kristian Fauchald and Don Reish for reviewing die manuscript.

REFERENCES

Dales. R.P.. 1962. — The polychaete stomodeum and the interrelation of the families of Polychaeta. Proc. Zool. Soc.

London . 139 : 389-428.

DESBRUYfcRES, D., & Laubier. 1... 1986. Les Alvinellidae, une famille nouvelle d’annelidcs polychetes infeodees aux

sources hydrothermalcs sous-marines: systematique. biologic et ccologie. Can. Journ. Zool.. 64 : 2227-2245.

FAUCHALD, K.. & Jumars, P.A.. 1979. — The diet of worms: a study of polychaete feeding guilds. Oceanogr. mar. Biol.

Ann. Rev., 17 : 193-284.

Fauvel, P.. 1897. Rceherches sur les Ampharetiens. Lille, Imp. L. Danel. 230pp.

FOURNIER. J.A.. & PETERSEN. M.E.. 1991. — Cossura longocirrata : redescription and distribution with notes on

reproductive biology and a comparison of described species of Cossura (Polychaeta. Cossuridae). Ophelia. Suppl. 5 :

63 -80.

HOLTHE T.. 1986. — Evolution, systematics and distribution of the Polychaeta Terebellomorpha, with a catalogue of the

Taxa and a Bibliography. Gunneria. 55 : 1-236.

PURSCHKE, G., 1984. — Vergleichende analomische und ultastrukturelle Unlersuchungen vcntraler Pharynx Apparaie bei

Polychaelen und ihre phylogenetische Bedeutung. Ph. D. Diss., GotUngen, 372pp.

PURSCHKE., G.. 1985. Anatomy and ultrastructure of ventral pharyngeal organs and their phylogenetic importance in

Polychaeta (Annelida). 2. The pharynx of Nerillidae. Mikrofauna Mar.. 2 : 23-60.

PURSCHKE., G.. 1987. Anatomy and ulUastructure of ventral pharyngeal organs and their phylogenetic importance in

Polychaeta (Annelida). 4. The pharynx and jaws of the Dorvillcidae. Aela Zool.. Stokh.. 68 : 85-105.

PURSCHKE., G.. 1993. — Structure of the prostomial appendages and the central nervous system in the Prolodrilida

(Polychaeta). Zoomorphology. 1 13 : 1-20.

SUTTON, M.F.. 1957. — The feeding mechanism, functional morphology and histology of the alimentary canal of

Terebella lapidaria L. Polychaeta). Proc. Zool. Soc. Ixrnd., 129 : 487-523.

TTlULIN, G.. 1921. — Biologisch-faunistische Untersuchungen aus dem Vresund. VI. Uber Cossura longocirraia Webster &

Benedict und uber die Rohren von Disoma multiselosum Oersted. Lunds Univ. Ersskr. N.F.. Avd. 2, Bd.17. 10: 2-15.

TZETLIN, A.B., 1981. — Fauna and distribution of the polychaetes of the White Sea. Ph. D. diss., Moscow, 1- 355 (in

Russian).

TZETLIN, A.B.. 1991. — Evolution of the feeding apparatus in the order Capitellida (Annelida. Polychaeta). Zool. Zhurn..

70 : 10-22 (in Russian).

Source : MNHN. Paris

16

Polychaetes of the Family Acoetidae (= Polyodontidae)

from the Levant and the Central Mediterranean with

a description of a new species of Eupanthalis

M.Nechama BEN-EUAHU* & Dieter FIEGE **

’ The Life Sciences Collections, The Department of Evolution, Systcmatics and Ecology

The Alexander Silberman Institute of Life Sciences

The Hebrew University of Jerusalem, 91904 Jerusalem

**Forschungsinstitut und Naturmuseum Scnckenberg

Senckenberganlage 25. D-60325 Frankfurt am Main, Germany

ABSTRACT

Five species of Acoetidae are present along the Mediterranean coast of Israel: Eupolyodontes cornishii Buchanan. 1894. a

new record for the Mediterranean and. probably, only the second finding of this species since its description from the mouth of

the Congo River (Africa); Euarche tubifex Hhlers, 1887, also found off Sicily; Polyodontes maxillosus (Ranzani. 1817).

comparatively rare; Panthalis oerstedi Kinberg. 1856 found in deeper waters off the Mediterranean coast of Israel than

previously recorded; and Eupanthalis glabra . n.sp.. from Israel and Cyprus. The new Eupanthalis species can be distinguished

from another Mediterranean species, E. kinbergi McIntosh. 1876. by its smooth rather than papillate palps. The relationship of

body size and depth, and differences in body size between Levant and central Mediterranean populations arc discussed.

RESUME

Polychetes de la famille des Acoetidae dc la Mediterranee levantine et centrale avec la description d'une nouvellc

espece du genre Eupanthalis

Cinq especes de la famille des Acoetidae sont presentes le long des cotes mediterranccnnes israeliennes : Eupolyodontes

cornishii Buchanan. 1894 nouvellc pour la Mediterranee et, probablcment, retrouvee pour la deuxieme fois depuis sa

description originate dans 1’estuaire du Congo (Afrique); Euarche tubifex Ehlers. 1887 egalement trouvee en Sicile;

Polyodontes maxillosus (Ranzani. 1817), comparalivement rare; Panthalis oerstedi Kinberg. 1856 trouvee plus profondement

que lors des recoltes precedenles; et Eupanthalis glabra . n. sp.. trouve en Israel et a Chypre. Cette nouvelle espdee

d' Eupanthalis se distingue de l’aulre espece meditenaneenne. E. kinbergi McIntosh. 1876, par ses palpes lisses depourvus de

papilles. Des relations entre les dimensions du corps et la profondeur de recolle ainsi que les differences de taillc entre les

populations lcvantines et celles de Mediterranee centrale sont discutecs.

BEN Eliahu, M.N. & D. Fiege, 1994. - Polychaetes of the Family Acoetidae (= Polyodontidae) from the Levant and the

Central Mediterranean with a description of a new species of Eupanthalis. In: J.-C. Dauvin, L. Laubier & D.J. Reish (Eds).

Actcs de la 4emc Conference internationale des Polychetes. Mem. Mus. natn. Hist, nat .. 162: 145-161. Paris ISBN 2-85653-

214-4.

Source : MNHN. Paris

146

M.N. BEN ELIAHU & D. FIEGE

INTRODUCTION

The present paper reports on aphroditoid polychaetes of the family Acoetidac Kinberg, collected between

1968 and 1991 in die Levant Basin off the Mediterranean coasts of Israel and Sinai, and off Cyprus, and in the

central Mediterranean off Sicily. Acoetid scaleworms are among the largest polychaete species. They are

characterized by parapodial organs (spinning glands) which produce fibers to build permanent felt-like tubes

packed with clay (Fig. 7a). Acoetids are carnivorous and have powerful jaws (Figs 2d,e: 6b; 9b). Some species are

rarely recorded. Some penetrate to batliyal depths.

A single worm, belonging to the giant species, Eupolyodontes cornishii, was collected off Ashqelon in 55 m by

E. CilLAT and G. Sachnin in 1969. The identification to species was made by comparison with the hololype. The

recent revision of die family Acoetidae by PETTIBONE (1989) enables an appreciauon of die rarity and importance

of this find (Ben-Eliahu & Fiege, 1991); it appears to be the second record since the holotype was described by

Buchanan (1894) from die moudi of die Congo River. Recendy, J. Nunez has found E. cf. cornishii off Tenerife

(NUNEZ, pers. comm.).

Petti BONE's revision (1989) led to recognition of a second, undescribed, Mediterranean species of Eupanthalis

along die coastal shelves of Israel and Cyprus, and it is described below as Eupanthalis glabra , sp. nov.

A gradiud accumulation of acoetid material has come from increasingly deeper sampling off die Mediterranean

coast of Israel, carried out by different projects and institutions: die joint project "Biota of the eastern

Mediterranean and Red Sea" of the Hebrew University of Jerusalem and Smidisonian Institution (H. STEINITZ,

F. D. Por and W. Aron [discussed in Por et ai, 1972]); die Sea Fisheries Research Station, Haifa (E. Gilat); Tel

Aviv University (Ch. Lewinsohn, M. Tom and B. Gaul); die 'Meteor' V expedidon (M. Turkay) obtained some

particularly rich samples of Acoetidae (for stations, see WE1KERT, 1988). Subsequent deep sampling cruises of

polludon monitoring off the northern Israeli coast carried out by S. PlSANTY and D. Golani (Israel Department of

Fisheries and Hebrew University of Jerusalem, respectively); and B. Galil (The Israel Oceanographic and

Limnological Research, Ltd.), have occasionally brought up Panthalis oerstedi (Ben-Eliaiiu, 1990; Ben-Eliahu

et ai, 1991). The combined data provide dcpdi distribution profiles of diese species along die Mediterranean coast

of Israel.

Recently, die 'Poseidon' 172—4 expedition of die Geologisch-Palaontologisches Institut und Museum, Univ.

Kiel to presumed hydrodiermically acuve sites off Sicily (PUTEANUS, 1990), collected Euarche tubifex.

MATERIALS AND METHODS

The samples: samples are listed in Table 1; for Levant sites, see fig. 1 and for Sicilian sites see PUTEANUS,

1990. Abbreviations in die sample codes are as follows: (I) Israel or Cyprus. (TAU) Tel Aviv University; (SFR)

Sea Fisheries Research Station, Haifa; (SLMB) sample of "Biota of die Red Sea and eastern Mediterranean" (POR

et ai, 1972); (SMF) Senckenberg-Museum, Frankfurt; (GPK) Geologisch-Palaontologisches Institut und

Museum, Univ. Kiel; (IOLR) Israel Oceanographic and Limnological Research, Co., Ltd.

Repository of specimens is as follow: I-coded material is at die Hebrew University of Jerusalem (ITUJ); S-

coded material is at die Senckenberg Museum, Frankfurt (SMF). Also, (AMS) Australian Museum, Sydney;

(BMNH) Natural History Museum, London; (MNHNP) Museum National d'Histoire Naturelle, Paris; and

(USNM) National Museum of Natural History, Washington.

Measurement of preserved specimens: for population lengdi comparisons, we used 11+10 (die prostomium and

tentacular segment plus following 10 sedgerous segments), which enabled using fragmented as well as complete

specimens as suggested by K. Fauchald (pers. comm.).

The following data were recorded: (1) Condition of specimen: complete/ anterior fragment/ middle fragment/

posterior fragment; (2) length in mm per number of segments (seg.); (3) length of 11+10 in mm; (4) width in mm

to edge of parapodia without setae, measured at widest part of body; (5) proboscis length (only if extended)

measured from base of prostomium and (6) t, number of teedi on each of the 4 jaws. In addition, for Eupanthalis

glabra , n. sp., relative lengdi of head appendages, as follows: tentacular cirri/ lateral antenna, tentacular cirri/

palps, lateral antenna/ prostomium, palps/ height of prostomium, tentacular cirri/ height of prostomium, length of

proboscis/ height of prostomium; nuchal fold present, absent or not visible due to position of head when

preserved.

Source :

ACOET1DAE FROM THE MEDITERRANEAN WITH DESCRIPTION OF A NEW SPECIES

147

Table I . — Samples collected off Mediterranean coast of Israel, Cyprus and Sicily

1I-IOLR. Haifa, 33°0TN, 34°34.2'E, L3: 1356 m. beam trawl L3; 5. XI. 1990; very rich in rocks and porous

metal either volcanic or industrial slag broken up; coll. S. Pisanty & D. Golani.

2I-IOLR. Haifa, LI- 33°02’01"N, 34° 29 E; 1,470 m, LI; 16.XI1.1992; coll. B. Galil.

3I-IOLR. Atlit; 200 m, beam trawl; 30.1.1990: coll. B. Galil.

41-lOLR. Atlit; 500 m, beam trawl; 31.1.1990; coll. B. Galil.

5I-IOLR. Atlit; 1,000 m, beam trawl; 31.1.1990, coll. B. Galil.

6I-SFR1610. Tantura, Gilat st. 17; 1 10m, dredge A; 3.IV.1968; coll. E. Gilat.

7I-SLMB1 13. Off Alexander River; 123 m, beam trawl; 26.IX.68, coll. G. Sachnin & M. Rapaport

8S-SMF. Jaffa, 32°02.38'N, 34°35.05'E - 32°00.95'N, 34°34.52'E, 'Meteor' V St. 50; 95-103 m, beam

trawl; 26.1.1987; coll. M. Tiirkay.

9S-SMF. Jaffa, 32°00.53'N, 34°33.98'E,'Mcteor' V St. 50; 1 10 m, grab; 26.1.1987; coll. M. Tiirkay.

10S-SMF. Jaffa. 32°01'N. 34°31.4'E — 31°58.9'N, 34°27.3'E, "Meteor" V St. 51; 309 m, beam trawl-

26.1.1987; coll. M. Tiirkay.

1 1S-SMF. Jaffa, 32°19.96'N, 34°31.46'E - 32°19.75'N, 34°31.26’E, 'Meteor' V St. 56; 694-700 m beam

trawl; 27-28.1. 1987; coll. M. Tiirkay.

12I-TAIJ. Palmachim; 35 m; 24-26.XI.1977; coll. B. Galil.

131-TAlJ. Palmachim; 35 m; 5-6.XI.1987; coll. B. Galil.

I4I-SLMB 156. Nabi Yunis (Aslidod); 128 m, beam trawl; 20.XI1.1968; coll. C>. Sachnin & M. Rapaport.

151-SLMB 157. Nabi Yunis (Aslidod); 128 m, dredge B; 20.XII.1968; coll. G. Sachnin & M. Rapaport.

16I-TAU. Nitsanim; 35 m; 28.11.1987; coll. B. Galil.

17I-TAU. Nitsanim; 80 in; 2.1V. 1977; coll. B. Galil.

181-TAD. Nitsanim; 80 m; l.VII. 1977: coll. B. Galil.

I9I-SFR1718. Ashqelon; 201 m, beam trawl; 30.X.1968; coll. G. Sachnin.

20I-SFR. 1742- Ashqelon; 55 m, knife dredge; 7. IV. 1969; G. Sachnin.

21I-SLMB6046. Sinai, Gaza; 36.6 m, beam trawl; 7. 1.70: coll. G. Sachnin.

22I-SLMB6021. el Arish; 137 m, dredge B; 27.VI11.1969, coll. G. Sachnin.

23I-SLMB6023. el Arish; 183 m, dredge B; 24.IX.1969, coll. G. Sachnin.

24I-SLMB6024. el Arish; 183 m, beam trawl, 27.VI1I.1969, coll. C>. Sachnin.

25I-SLMB 178. Sinai, Kalib el Galss (Bardawil); 91.5 m, beam trawl; 4.11,1968, coll. E. Gilat.

261 -SLMB 1545. Cyprus, Famagusta F; 100-110 m, dredge A; 16.11.1968. coll. A. Lurie.

27S-GPK. Graham Bank. 37°09.135'-37°08.90'N, 12o42.90'-12°43.23'E, "Poseidon" 172-4: 185-178 m.

Chain dredge; 2.V. 1990; coll. M. Tiirkay; #645.

28S-GPK. Cimotoe, 37°00.43'-37°00.45'N. 1 2°39.06’- 12°39. 1 l'E, "Poseidon" 172-4; 198-158 m, chain

dredge; 7.V. 1990; coll. M. Tiirkay, #718.

29S-GPK. Cimotoe, 37°00.20’-36°059.82’N, 12°39.08'-12°38.58'E, "Poseidon" 172-4; 224-230 m, chain

dredge; 2.V. 1990; coll. M. Tiirkay, #629.

30S-GPK. Cimotoe, 36°59.82'-36°058.37'N. 12°39.28'-12°39.90'E, "Poseidon" 172-4; 237- 220 m, chain

dredge; 2. V. 1990, M. Tiirkay; #630.

31S-GPK. Cimotoe. 36°059.38'N, 12038.74-E, "Poseidon" 172-4; 214-230 m, Van Veen grab; 1.V.1990;

__co]L M, Tiirkay; #620, _

Statistics were computed by the S AS statistical package. Description of new species gives: holotype parameter

(population mean ± s.d. [range], for N, number of individuals). To conform with Pettibone (1989), the text refers

to segments rather than setigers; in Aphroditoidea the first parapodium bearing setae is the 2nd segment.

Scanning Electron Microscopy (SEM): samples were dehydrated via graded ethanol series, critical-point dried

using C02 and examined in a CAMSCAN-SEM (CS 24).

Source :

148

M.N. BEN ELI AH U & D. FI HOE

FIG. 1 . Sampling sites off Israel (Haifa to Ashqelon) and northern Sinai (Gaza - Bardawil). Black star

white star, Eupolyodontes comishii.

33°

32°

31°

, Eupant kalis glabra ;

Source : MNHN, Paris

ACOETIDAE FROM THE MEDITERRANEAN WI TH DESCRIPTION OF A NEW SPECIES

149

SYSTEMATIC SECTION

Genus Eupanthalis McIntosh, 1876

PErriBONE, 1989: 24.

Eupanthalis glabra , new species

(Figs 2-5)

Material examined. — Samples: 61 (FIG. 2a): 71; 8S, Holotype and 66 paratypes; 9S; 141; 151: 221; 231; 251;

261 (Table 1). Total: 76 specimens, Cyprus, 1; Israel, 75.

REPOSITORY. — Holotype (HUJ). Paratypes: 23 (1IUJ); 24 (SMF 4430); 2 (AMS: W208889, W20890); 7 (BMNII

ZB 1992.305-311); 9 (USNM 157612, 157613, 157614); 2 (MNHNP: UC343-A922, 344-A922) Topoivpe- 1

(SMF 4431). *

Fig. 2. — Eupanthalis glabra, n. sp.: a, anterior end with fully everted proboscis (from Cyprus); b-e (from Israeli coast): b,

anterior end with fully everted proboscis (holotype); c, dorsolateral view of anterior end (paratype); d, frontal view of

proboscis; c, lateral view of same. (Scales, a-e = 1 nun)

150

M.N. BEN ELI AH U & D. F1EGE

Description. — Body elongate. Largest, complete specimen, 65 mm, 64 seg.; H+10, 2.3 mm; width, 3.5 mm.

Hololype (Figs 2b, 3a-j) anterior fragment with pharynx fully extended, 32mm /50 seg. (11+10, 3.0 mm), width

4.0 mm. Population, H+10, 2.8 ± 0.6 nun [2.0- 4.0 mm], N= 20 ; width, 3.5 ± 0.4 mm [2.8-4.0], N= 20.

Fig. 3. Eupanthalis glabra, holotype: a, head; b, left elytrigerous parapodium from segment 2. anterior view; c, left

cirrigerous parapodium from segment 3, anterior view; d, right parapodium from segment 48. anterior view; c, upper

neuroseta from segment 2 ( 1st parapodium); f, lower neuroseta of same; g, upper neuroseta of segment 3; h, middle aristatc

acicular neuroseta from same; i, aristate acicular setae with subdistal tuft from segment 10; j, capillary setae with circlets

of spines (type b) from same. (Scales: a = 1 mm; b-d, 100 pm; e-j, 50 pm).

Source :

ACOETIDAi; FROM THE MEDITERRANEAN WITH DESCRIPTION OF A NEW SPECIES

151

Elytra smooth, elongate-oval, delicate; first pair covering prostomium, second and third covering dorsum,

remainder leaving middorsum uncovered. Posterior elytra very delicate, with lateral pouches.

Prostomium oval, bilobed, with median longitudinal groove (Figs 2c; 3a; 4a-b), with two pairs of sessile eyes,

anterior pair much larger or only slightly larger than posterior pair. Lateral antennae with short ceratophores on

anterior side of prostomium, with tapered styles, 1.7 (1.7 ± 0.3 11.3-2.2], N=17) times longer than prostomium

Palps ventro-lateral to antennae, stout, tapered, smooth, 5.0 (3.4 ± 0.9 mm [2.2-5. 3 mm]. N=19) times longer than

prostomium (Figs 2a-c; 3a).

First (tentacular) .segment distinct dorsally; nuchal lobe observed on holoiype (Figs 3a. 4b); tentaculophores

lateral to prostomium, each with aciculum, without setae, with dorsal and ventral tentacular cirri subequal in

length, 2.2 (2.2 ± 0.4 [1.6-3.3], N= 20) times longer than prostomium, 1.3 (1.3 ± 0.3 [1.0-2 1] N= 17) times

longer and stouter than lateral antennae, and 0.4 (0.7 ± 0.2 [0.4-1 .0], N= 19) shorter than palps (Fig’s 2a-c: 3a; 4b).

FIG. 4. — Eupanthalis glabra , scanning electron micrographs: a, anterior end. dorsal view, b, same, view more frontal, c, right

parapodia of segments 2 and 3. anterior view, d, right parapodium of segment 3 . posterior view. (Scales: a = 1000 pm; b,

d = 300 pm ; c = 1 00 p m ).

Second segment (first setiger) with first pair of elytrophores: parapodia modified, paw-like, sometimes directed

anteriorly, with ventral buccal cirri similar to tentacular cirri, 2.5-3 (N= 2) times longer than following ventral cirri

152

M.N. BEN ELI AH U & D. FIEGE

(Figs 3b-c; 4c-d); notopodium small, rounded acicular lobe on anterodorsal side of larger neuropodium;

neuropodium without notosctae. with bilobed presetal acicular lobe.

Extended proboscis 6.9 (7.3 ± 1.8 [5.2-10.31, N=19) times longer than prostomium (Figs 2a-b-c). Distal border

of proboscis with 13 pairs of conical papillae, middorsal and midventral ones very slightly enlarged both on wide

bases with lateral curved tips (Fig. 2d-e); two pairs of strong honey-colored hooked jaws, each with 2-6 teeth

(holotype with 4,3, 3, 3 teeth), with opposite pattern of dentition in upper left and lower right jaws vis a vis lower

left and upper right jaws (Figs 2d-e).

Fig. 5. — Eupantlialis glabra, scanning electron micrographs: a-c. Neurosetae of segment 2: a. upper, posterior view; b,

same, anterior view; c, lower, anterior view; d, neurosetae of segment 3: left, middle aristate acicular; right, upper

lanceolate; e, neurosetae of segment 10: left, middle aristate acicular with subdistal brush; right, upper, type b capillary; f,

lower neuroseta of segment 4; g. setae of segment 10 from anterior, showing Fine fibers of spinning gland. (Scales: a-d. f =

30 pm; e, g = 100 pm).

Dorsal cirrus on segment 3 with short cirrophore on posterodorsal side of notopodium, with long tapered style,

1.7-2. 3 (N= 4) times height of parapodium, 1.8-2. 3 (N= 2) times longer than ventral cirrus (Figs 3c; 4c-d).

Source :

ACOETIDAE FROM THE MEDI TERRANEAN WITH DESCRIPTION OF A NEW SPECIES

153

Beginning with segment 9, notopoclium wider, rounded flattened, on anterodorsal side of neuropodium with

internal spinning glands. Middle parapodia with dorsal cirri short, slightly shorter than height of parapodium 1 5

tunes shorter than tapered ventral cirri (Fig. 3d). 1 1 ’

Far posterior region with notopodia reduced to conical lobes; neuropodia more elongate, narrower cirri longer

than in anterior region. Integument of posterior region very thin. Parapodial branchial tubercles (as in Fig. 8a) not

present. Pygidium small, rounded, between few posterior small segments with two anal cirri.

Notosetae present from segment 9 to 19-22, very fine setae with one spiny margin emerging from lower side of

notopodium (lug 5g). Neurosctae show some anterior-posterior transition in anterior-most parapodia Neurosetae

in three groups (upper with shafts above aciculum; middle with shafts above and below aciculum- lower with

shafts be low aciculum). Upper neurosetae of two types: type a longer, slender, somewhat lanceolate with spinous

margins (lugs 3e, g; 5a-b-d). present throughout body; increasingly finer and longer posteriorly (in segment 2 ca

1.7 times thicker than m segment 3); type b very line, shorter, with circlets of few widely spaced spines (Figs 3f

5c), lacking in anterior and posterior parapodia.

Middle neurosetae acicular with tips slightly hooked, bearing distal hairy aristae, on segments 3-8 without

subdistal tufts of spines (Figs 3h; 5d); from segment 9 on with subdistal tuft (Figs 3i; 5e).

• L°^r curved’ wiUl Proximal spines on one margin, tapering distally to circumferential, close-set

spines (Figs 31; 5c-f).

Second segment Hirst setiger, lugs 3b; 4c): upper neurosetae, somewhat lanceolate with spinous margins more

massive than in following parapodia, 6 (6-7, 6.3 ± 0.6, N= 4 [Figs 3e: 5a-b]). Lower, 6 (1-6, 3.5 ± 2.1, N= 4 [Figs

Third segment (Figs 3c: 4d): upper neurosetae, 2 (1-2, 1.8 ± 0.4, N= 5), 0.3 (0.3-0.6) times as thick as in 2nd

segment (lugs 3g; .id. right). Middle aristate acicular neurosetae, 6 (5-6, 5.6 ± 0.5, N= 5, lacking subdistal spines

(Figs 3h; 5d, left), 2.2 (4) times as thick as upper. Lower neurosetae, 35 (14-35, 18.4 ± 9.3, N= 5 [Fi»s 3c. 4d[

with fine shafts ca. 1/4 those of upper neurosetae.

_ Fwm and including segment 9: upper neurosetae, type a, 18 [ 13-21, 16.4 ± 2.9] N= 7); type b, 31 [25-42, 32.1

± 5.5] N=7 (Figs 5e-g). Middle acicular neurosetae with subdistal spines, 7 [1-7, 5.7 ± 1 9 N=6] (Fi«s 3F 5e)

Lower neurosetae, 16 [7-16, 12.3 ± 3.3] N= 7 (Fig. 50.

Distribution. Cyprus ( 100-1 10 m), Israel (91.5-183 m [Fig. 1]); note the narrow depth range (Fig. II).

Etymology. — From die Latin, "glaber" meaning smooth, referring to the smooth palps.

Remarks. Pettibone (1989: 241) redescribed Eupanthalis kinbergi according to McIntosh (1876) and

supplemented the description of die holotype, whose palps were missing, with that of a specimen from Naples

McIntosh did not mention die palps.

As die present material shows, dierc are two species of Eupanthalis in die Mediterranean, one widi papillated

palps and one with smooth palps. Unfortunately, since die palps are missing on the holotype and not mentioned by

McIntosh, there is no possibility of ascertaining whether or not E. kinbergi indeed had papillated palps. We

propose that the name kinbergi be retained for the species with die papillated palps, as redescribed in Pettibone

(1989) and the new name, glabra, be applied to the Levant species with smoodi palps. Another difference between

diese species is the color of the jaws, dark in E. kinbergi, honey-colored in E. glabra. E. glabra is of much smaller

size than E. kinbergi. The presence or absence of a nuchal lobe is a difficult character to determine in this

preserved material; it appears to be present in E. glabra (Figs 2a-c; 3a; 4b).

Pettibone (1989) refers to two additional species widi smoodi palps; E. edriopthalma (Potts 1910) from the

Western Indian Ocean and E. elongata (Treadwell, 1931) from die Philippine Islands; bodi species have the

tentacular cirri about as long as die palps (in E. glabra, die tentacular cirri are shorter than the palps); both species

lack a nuchal lobe. E. edriopthalma has much shorter palps relative to the height of the prostomium than E glabra

(syntypes of E. edriopthalma with palps 1.1 ± 0.2 [1.0-1 .3, N= 2[) times longer than prostomium). Within die type

sample containing 67 individuals, the E. glabra population showed considerable variability in the relative lengths

of the head appendages (lengdi of palps vis a vis the antennae and the tentacular cirri, see Figs 2a-c). It may also

be related to the degree of contraction when preserved. None of the 19 individuals measured showed the short

condition as in E. edriopthalma.

E. elongata has different neurosetae on segment two and dark jaws (PETTIBONE, 1989). It also has longer

antennae relative to the prostomium [N= 1]; only one of 19 specimens of E. glabra measured showed the long

condition as in E. elongata.

154

M.N. BEN ELI Mill & D. REGE

The present study points to die difficulty of comparing populations in which variability has been found with

species descriptions based on few specimens. This problem is particularly acute in deep-water species with sparse

material.

Euarche tubifex Ehlers, 1887

(Figs 6; 8e)

Euarche tubifex - PETTIBONE, 1989: 14-18, Fig. 15.

Eupanthalis kinbergi -Fauvel, 1923: 100-101, Figs. 38i-q; AMOUREUX, 1976: 1049

(Not Eupanthalis kinbergi McIntosh, 1876]

Material examined: samples: 31, 3x: 8S; 121; 131; 161; ?16I, 3x; 171; 211; 27S, lx (SMF 4428); 28S, lx (SMI-

4427); 29S. 4x (SMF 4426); 30S, 2x (SMF 4429); 31S (SMF 4425) (Table 1).

Total: 11 specimens from Israel, H+10 length, 5.5 ± 2.2 mm [3-10 mm], N= 9). Largest, AI-, 78 mm, 69

segments (H+10, length, 10 mm); width, 9 mm (from sample 112). Nine specimens from Sicily, H+10 length, 9.00

± 1 .32 mm [8-1 1 mm], N= 9). Largest, AF, 85 mm, 63 segments (11+10, 1 1mm); width, 15 mm; with eggs.

FIG. 6. — Euarche tubifex : a, specimen from Israel, dorsal view of anterior, proboscis fully extended; b. specimen from Sicily,

lateral view of same. (Scales: a. b = 1 mm)

Remarks. — A decapod belonging to the family Pandalidae (M. Turkay, pers. comm.) was removed from die

gut of a Sicilian specimen.

Distribution. — Sicily (158-237 m), Israel (35 - 200 m). Worldwide (Pettibone, 1989): Caribbean, Northwest

Atlantic from Florida to North Carolina, Gulf of Mexico, Panama (Pacific), Southwest Atlantic to South Brazil,

Northeast Atlantic from West to Northwest Africa, Mediterranean, Arabian Sea, 13 to 450 m.

Source :

ACOETIDAE FROM THE MEDITERRANEAN WITH DESCRIPTION OF A NEW SPECIES

155

Eupolyodontes cornishii Buchanan, 1894

(Figs 1; 7; 8a-c)

Eupolyodontes cornishii Buchanan 1894: 438, pi. 227: Figs 1-8. - Pettibonf., 1989: 36, Figs 20-22.

Material. Sample 201 (Table 1). Anterior fragment, 74 setigers, 230 mm (II+10, 22.7 mm)- width 27 8 mm

fragment ol tube. Permanent mounts I IUJ-#361, 367: SMF-SHM #30.

FlO. 7. Eupolyodontes cornishii: a. tube after washing out interwoven clay; b. anterior fragment, dorsal view, with most

elytra missing; c. anterior end, dorsal view, with left lstelytrum pinned back. 1st right elytrum missing. (Scale: c= 1 mm).

Additional material studied. — Africa, off Congo River, 79-86 m, holotype (BMNH 1893.12.8.1).

Remarks. I he anterior fragment was inside the tube (Figs 7a, b). In her review of the Acoetidae, Pettibone

(1989) cites only the holotype; she considered another record of a New Caledonia specimen, deposited at (lie f’aris

Museum (Fauvel, 1897) as doubtful. The present material was collected in 1969 (Ben-Eliahu & Fiege, 1991)

and may be only the second record of E. cornishii since dial of Buchanan in 1894. J. NUNEZ has recently found

E. cf. cornishii from Tenerife from 200 m depth, based on a fragment of some middle setigers (J NuNEZ pers

comm.).

Ihere are some minor differences from the holotype redescribed by Pettibone, mainly in characters which

'aH w‘tl»n species variability; the description was based on a single specimen. The palps are short, but subequal in

length to the ventral tentacular cirri, and slightly surpass the prostomium. Notosetae were observed on the

tentacular segment and on segment 2 but not on segments 3 and 4.

Parapodial branchiae begin on segment 8 (rather than 6); most branchiae are simple, some with one branch (Y-

shaped. Fig. 8a), fewer with double-Y or with single and Y, best-developed between segments 17-31, and

continuing to the end of the fragment. The upper neurosetae (Fig. 8c, cf. Fig 22Ba of Pettibone, 1989) show a

slight swelling ("neck") at die proximal tuft and are somewhat recurved distally. This was confirmed on the

holotype.

156

M.N. BEN ELIAHU & D. F1EGE

Distribution. — Israel (55 m). Worldwide (Buchanan, 1894): Africa, mouth of Congo River, 35m from land,

79-86m; Tenerife, (200 m) (Nunez, pers. comm.) (55 - 200 m).

Fig. 8. — Scanning electron micrographs: a-c, Eupolyodonies comishii : a. 20th right parapodium, posterior view; note

parapodial branchiae; b, middle acicular neuroseta; c. upper neurosetae; d. Polyodontes maxillosus , middle acicular

neurosetae: e, Euarche tubifex : middle acicular neuroseta from 3rd segment, anterior view; f, Pcinlhalis oerstedi, tip of 9th

right neuropodium, left, middle acicular neurosetae; right, upper neurosetae. (Scales: a = 1,000 pm; b-d, f = 100 pm;

e = 60 pm).

Panthalis oerstedi Kinberg, 1856

(Figs 8f: 9a-c)

Panthalis oerstedi Kinberg, 1856: 387 - PETTIBONH, 1989: 53-56, Figs 32-34; BEN-EL1AHU el al. 1991: 62-64.

MATERIAL examined. — Samples II; 21; 31; 41, 5x; 51, 6x; 8S, lx(SMF4407); 10S, 6x (SMF4417); 1 IS. 8x

(SMF 4418) ; 191, lOx; 231; 241, 4x (Table 1). Total: 44 specimens, largest, anterior fragment, 18mm, 32

segments, H+10, 5 mm; width, 6.2 mm. Large complete specimen, 35 mm, 71 segments (11+10= 5.5): width 5

mm. H+10, 2.5 - 5.5 mm [3.6 ±0.8], N=41.

Source :

ACOETIDAE PROM THE MEDITERRANEAN WITH DESCRIPTION OF A NEW SPECIES

157

Remarks. Body broadens after about segment 16 and then narrows. Many individuals of sample 51 with

opaque dark brown bodies in body cavity, presumably parasites (Figs 9a,c). Figure 9c shows the long filament of

the spinning gland in die body cavity. The depdi range is extented to 1.470 m.

Fig. 9. a-c. Pcmthalis oerstedi. a, dorsal view of anterior; b. lateral view of anterior end with proboscis fully extended; c.

parapodium with elytron and long filament of spinning gland in body cavity; dark circles presumed to be cysts of parasite;

d. Polyodontes maxillosui: dorsal view of anterior end. (Scales: a-d = 1 mm).

DISTRIBUTION. — Israel (95 m - 1470 m). Worldwide (PirniBONE, 1989: 56): Sweden, Norway, North Atlantic to

Mediterranean, Northwest Africa (1 1 -760 m); die depdi range is broad, 1 1 - 1,470 m.

Polyodontes maxillosus (Ranzani, 1817).

(Figs 8d; 9d)

Polyodontes maxillosus. — Petobone, 1989: 101-103, Figs 70-72.

Material examined. — Samples 61; 8S (SMF 4421); 121 (Table 1). Total: three specimens, largest, anterior

fragment, 43 mm. 52 segments (11+10, 5 mm): width. 3 mm. 11+10, 3.6-5 mm [(4.2 ± 0.7) N= 3).

158

M.N. BEN ELI AI IU & D. FIEGE

DISTRIBUTION. — Israel (35-110 m). Worldwide (PETTI BONE, 1989): North Atlantic off Spain, Adriatic, Red Sea,

low water to 280 m.

FK3. 10. — Lengths of specimens of Euarche tubifex (11+10 parameter) vs. depth.

KEY TO THE LEVANT ACOETIDAE

1 Eyes stalked (ommatophores); 3 antennae (Figs 7; 9) .

Eyes not stalked, sessile; 2-3 antennae (Figs 2a-c; 6) .

2 Parapodia branchiae absent (Fig. 9d); palps well-developed (Fig. 9a-d);

acicular neurosetae aristate (Fig. 8d-f) .

Parapodial branchiae present (Fig. 8a); palps reduced (Fig. 7c);

neuroacicular; setae not aristate (Fig. 8b); of giant size . £• cornishii

3 Ommatophores white; sessile eyes absent (Fig. 9a);

upper neurosetae pcnicillate (Fig. 80 . P • oerstedii

Ommatophores black; sessile eyes present (Fig. 9d); upper neurosetae

tapered (Fig. 8d) . P • nioxillosus

4 Two antennae (Fig. 2a-c; Fig. 4a-b) . . . 5

Three antennae (Fig. 6a-b) . £• tubifex

5 Palps papillated . £• kinbergi 1

Palps smooth (Fig. 4a-b) . ; . gtabra

DISCUSSION

Mediterranean biogeographers have reported reduced body size (dwarfing) in several different groups in die

Levant marine fauna (sponges, echinoderms, sipunculids and polychaetes [e.g., LAUBIER, 19661). However, the

observation on dwarfing in the Levant has yet to be analyzed properly. Hie present paper describes differences in

length of specimens of Euarche tubifex from die Israeli and Sicilian coasts. The Israeli populadon was of smaller

size than the Sicilian one (Israel, H+10, 5.50 ± 2.17 mm [range, 3-10 mm], N= 9, vs. Siciliy, 11+10, 9.00 ±

1 Not found in Levant. Reported from Italy (Pettibone. 1989).

Source :

ACOETIDAE FROM THE MEDITERRANEAN WITH DESCRIPTION OF A NEW SPECIE S

159

1.32 mm [range 8-11 mm], N= 9) and llie difference between the means was significant (t-test, t= -4.1384,

p = 0.0008, Fig. 10). Information concerning the age of the specimens is lacking. In addition, die depth ranges

sampled may not be comparable: the Israeli E. tubifex population came from a broader range beginning0 in

shallower depths than die Sicilian one (35-200 m : 158-237 m, Israel : Sicily, respectively).

Fig. 11. — Levant (L) and worldwide (W. from PETTIBONE, 1989) depth distribution of aeoedd species: E.g.. Etipanthalis

glabra: P.o., Pamhalis oerstedi ; P.m.. Polyodontes maxillosus ; E.t ..Euarche tubifex: E.c.. Eupolyodontes comishii.

6

5.5

1 5

o 4.5

I 4

B)3,5

s 3

2.5

2

0 200 400 600 800 1000 1200 1400 1600

Depth (m)

Fig. 12. — Length of specimens of Panthalis oerstedi (11+10 parameter) vs. depth.

H+10 length (mm)

FIG. 13. Lengths (H+10) of Israeli Acoetidae. mean ± s.d; N. number measured.

Source :

160

M.N. BEN ELIAIIU & D. FIEGE

To evaluate whether populations from different depths can be compared requires determining whether a

positive correlation exists between depth and body size, as in gastropod populations from intertidal and subtidal

depths (Kohn. 1971; Kohn & Nybakken, 1975). Two species are rare, Eupolyodontes comishii , found only

once, and PolyodontesjnaxiUosus, found only three times. One species, Eupantiialis glabra, appears to have a

very restricted depth range (from 90-183 m. Fig. 1 1). Thus, the proposed correlations for body size and depth

could only be carried out for Euarche tubifex (Israel), and Pcinthalis oerstedi.

For Pcinthalis oerstedi , die deepest species (Fig. 11), and one with a great depth range (95 - 1470 m), the

Spearman correlation between length of specimens and depth was highly significant (r = 0.60500, p = 0.0001,

N= 41, Fig. 12). However, in the Israeli Euarche tubifex population, it was not significant (r = 0 32154 p= 0 3988

N= 9); the largest specimens were from die greatest depth (Fig. 10), however, die smaller worms were not only

iom die shallowest depth. The small depth range (165 m) or die small samplesize (N= 9) may contribute to this

lack ol significance. Unlortunately, on die basis of these results, body sizes of individuals from different areas

which come from different depths cannot be made.

A comparison ol the body sizes of die five Israeli species is given in Fig. 13. Depth distributions of the five

species along the Israeli coast are compared with their worldwide distributions given in PETTI BONE, 1989 (FF

1 1 ). Three of (he species' ranges begin in deeper waters in die Levant than elsewhere. This has previously bec^i

reported lor Levant serpulid Species (Ben-Eliahu. 1991). All four of die smaller species (Figs 1 1; 13) are present

and appear abundant at 100 in. As noted above, die Levant population of P. oerstedi is recorded from 1,470 m

700 in deeper than elsewhere (Fig. 11); die species appears to be abundant from 200 m.

ACKNOWLEDGEMENTS

We thank M. TOrkay of the Forschungsinstitut und Naturmuseum Senckenberg for samples of die 'Meteor' V

and die oseidon 1 72-4 cruises, and for identifying the decapod prey. Samples were made available by E. Gii.at

o the Sea fisheries Research Station; die project, "Biota of die Red Sea and eastern Mediterranean"; the Israel

National Collections of Natural History at Hebrew University and at Tel Aviv University lor loan of material- S

I 'san-i y, Department ol Fisheries. Ministry of Agriculture; D. C.OLANI, The Hebrew University of Jerusalem and

B. Gai.il. Israel Oceanographic Institute. Ltd.; J. Nunez for data. We also thank D. Gateno for assistance with

die statistical analysis: S. IlALBRElCH redrew Figure 3; A. Neev did some of the photographs. R. Barnich for

Fruie h translations; M.L. I RITZ tor invaluable assistance. D. GEORGE and A. Muir for a productive visit to the

British Museum (Natural History). H. BROMLEY-SCHNUR, M. TOrkay, F.D. Por read previous drafts; two

anonymous reviewers made valuable suggestions.

KbII-KLNCFS

AM“!- IX- ‘ israelitica. nouvelle espece dc Serpulidae (Annelidas Polychcles) el une petite

collection annehdienne de la Mediterranee orientale. null. Mus. nail Hist. not. Pahs. 3 ser.. 404 : 1047-1059.

“r- M'N'T11990' ,Sccond preliminary report on Polychaeta from some deep-sea benthic sampling in the eastern

SSnea,nT fCt| 'i MaR™ & B- °AUL Proc. Second Interdisciplinary Conference on L Continental

SlelJ of Israel. I el Aviv University. May, 1990. Inst, for Nature Conservation Research. Tel Aviv University : 28-29.

BEN-ELlAltu. M.N., 1991. — Red Sea serpulids (Polychaeta) in the eastern Mediterranean, pp. 515-528. Ophelia. Suppl.. 5 :

Bl^TtM N-; M',N. * fIEGE: l99L ~ Somc sPecies belonging to the Aphroditoid family Acoetidae (Polychaeta)

horn the Levant and the Central Mediterranean. Abstracts of the Israel Zool. Soc. Meeting. Dec. 2-3. 1991. Tel Aviv : 1 1 -

BEN-EL. AHU. M.N F.D. Por & B. GaLU.. 1991. - A preliminary report on the density and composition of small sbe

Levantine bathyal benthos. Abstract. In : Y. Marth & B. Galii. (eds), Proc. Third Annual Symposium on the

Medttertanean continental margin of Israel. Israel Ocean. & Limn. Res,, Nat. Inst. Oceanogr. ; 62- 64. ' P

BUCHANAN. F.. 1894. - A Polynoid with branchiae ( Eupolyodontes comishii ) Quart. J. Microsc. Sci. (Loud.), 35 : 433-450.

88-n2erVali0nS SUF lEup0ly0d0n,eS cM“ Buchana„ (Annelide Polychete Errante). null. Soc. Linn.

Source : MNHN, Paris

ACOETIDAE FROM THE MEDITERRANEAN WITH DESCRIPTION OF A NEW SPECIES

161

FauVEL. P.. 1923. — Polych&tes Emmies. Faunc de France 5 : 1-494.

Kinberg. EG. FI., 1856. Nya slagten och arter of Annelida. K. Vetensk.-Akad. Fo>/i.(Stokholm). 12 : 381-388.

Kohn. A.J 1971. — Diversity and utilization of resources and adaptive radiation in shallow-water marine invertebrates of

tropica] oceanic islands. Limn. Oceanogr .. 16 : 332-347.

Kohn. 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. 1

LAUBIER, L., 1966. Sur quelques Annelides Polychctes de la region de Beyrouth. Am. Univ. Beirut Miscell. Pap.. 5 : 9-22.

MCl4™SH W C * 1876 ~ °n lhC Annelida °f ^ PorcuPine Expedition of 1869 and 1870. Trans. Zool. Soc., Lond.. 9 : 395-

PETTIBONE, M.H.. 1989. Revision of the aphroditoid polychaetes of the family Acoetidae Kinberg (= Polyodontidae

Augener) and reestablishment of Acoeies Audouin and Milne-Edwards. 1832 and Euarche Ehlcrs, 1887 Smiths Conir

Zool.. 464 : 1-138.

POR. P.D.. H. Steinitz, I. Ferber & W. ARON. 1972. — The biota of the Red Sea and the Eastern Mediterranean (1967-1972)

A survey of the marine life of Israel and surroundings. Isr. J. Zool.. 21 : 459-524.

Potts, F.A., 1910. — Polychaeta of the Indian Ocean. Part 2: The Palmyridae.

Sigalionidac. Trans. Linn. Soc., London, scr. 2. 13 : 325-353.

Aphroditidae, Polynoidae, Acoetidae, and

PUTEANUSD., 1990. - Cruise Report 'Poseidon' 172 4. MIPAMEHR-MAST I. Volcanism and Hydrothermal Activity in the

Strait of Sicily. Malaga Trapani - Faro, 19.4.-14.5.1990. Reports. Gcol.-PalSont. Inst Univ. Kiel. 41:1-1 16.

TREADWEl-L. A.L., 1931. — Four new species of polychaetous annelids collected by the United States Fisheries Steamer

Albatross during the Philippine Expedition of 1907- 1910. U.S. Nat. Mas. Bull., 100, 6 : 313-321.

Weikert, IT. 1988. — Expeditionsbcricht fiber die "Meteor" -Reise 5, Abschnitt 1. (2. Januar bis 28. Januar 1987 Ostliches

Mittelmeer/ Hamburg Heraklion - Port Said). Inst. f. Hydrobiologie und Fischereiwissenschaft. Berichte aus dent

Zentrumf Meeres- und Klimaforschung der Universitat Hamburg'. 1-39.

Source : MNHN. Paris

17

Prionospio caspersi Laubier (Polychaeta, Spionidae)

in the Black Sea: long-term monitoring

of a population

TemirA. BRITAYEV * Alberto CASTELU** & Tatiana S. AKSIUK*

* A.N. Severtzov Institute of Evolutionary Animal Morphology and Ecology

Russian Academy of Sciences

Leninsky prospect 33, Moscow 1 17071, Russia

** Istituto di Scienze Antropologiche, University di Sassari

Corso Margherita di Savoia 15

1-07100 Sassari, Italy

ABSTRACT

Numerous specimens of the spionid polychacte Prionospio caspersi Laubier were found in benthic samples from Kapsel

Bay. the southeastern coast of the Crimean Peninsula. This was the first record of this species in the Black Sea. P, caspersi was

very abundant in sandy and silty sand communities at depths of 9 to 23 m. We monitored this community from 1986 to 1991, a

period in which the density of P. caspersi varied seasonally, being highest in spring (up to 730 ind. m2) and decreasing in the

months of August and September (to 96 ind. m2). From April 1986 to April 1989. the frequency of occurrence in grab samples

varied from 50 % to 100 %. decreasing at the end of each summer. Interpretation of size-frequency histograms suggests that

recruitment look place in the second half of the summer. In autumn 1989 P. caspersi disappeared from Kapsel Bay and was not

found at the study site or adjacent areas in 1990 or 1991. Possible causes for its disappearance were discussed.

RESUME

Prionospio caspersi Laubier (Polychaeta, Spionidae) en mer Noire : suivi a long ternie d’une population

De nombreux exemplaires du polychete spionide Prionospio caspersi Laubier ont ete recueillis sur les fonds de la baie de

Kapsel. sur lc cotes du Sud-Est de la Crimee, mer Noire. II s’agit de la premiere decouverte de cette espece en mer Noire. P.

caspersi apparait avee une tres grande abondance sur les fonds sableux et sablo-vaseux entre 9 et 23 metres de profondeur.

Nous avons suivi cette communauhS de 1986 a 1991. periode au cours de laquelle la densite de P. caspersi a varid selon les

saisons, atteignant au printemps son maximum (jusqu'a 730 ind. m2) et diminuant ensuite dans les mois d’aoGt et de septembre

(a 96 ind. m2). D'avril 1986 a avril 1989, sa frequence dans les echantillons a vari£ de 50 % a 100 %, diminuant a la fin de

chaquc ete. L' interpretation des histogrammes taille-frcquencc suggere que le recrutement advient dans la seconde moitic de

l'cte. Au cours de l automne 1989, P. caspersi a disparu de la baie de Kapsel, aucun exemplaire n'ayant ete retrouve ni en 1990.

ni en 1991. Les causes possibles de cette disparition sont discutees.

BRITAYEV. T.A.. CASTELU, A. & T. S. AKSIUK, 1994. Prionospio caspersi Laubier (Polychaeta, Spionidae) in the Black

Sea: Long-term Monitoring of a population. In: J.-C. DaUVIN. L. LAUBIER & D.J. REISH (Eds). Actes de la 4cme Conference

internationale des Polychetes. Mem. Mus. natn. Hist, nat., 162 : 163- 168. Paris ISBN 2-85653-214-4

Source : MNHN. Paris

164

A BRITAYEV. A. CASTELLI & T. S. AKSIUK

INTRODUCTION

Prionospio caspersi Laubier, 1962 was first discovered in Venice Lagoon (Laubier, 1962) and later found in

many areas of the western Mediterranean and Adriatic seas (Laubier, 1965; GuBrin, 1970). This species inhabits

sand and silty-sand sediments of the upper sublittoral zone (I.ardicci, 1989). In die Black Sea. P. caspersi was

recently found and described from the southeastern coast of the Crimean Peninsula (Britayev et al, 1991, Fig.

1). In this paper we suggested that P. caspersi had earlier been misidentified as P. malmgreni Clapaitde, 1868 and

that its distribution in the Black Sea was thus probably considerably wider than realized.

FiG. 1. — Study area in Lapse! Bay, the Black Sea. Sampling stations (A-K) indicated by black dots. Shaded areas show

location of mussel (Mytilus galloprovincialis ) farm.

1 lie ecology ol P. caspersi in the northern Adriatic, mainly its secondary production in the vicinity of the Po

Estuary, was investigated by Ambrogi el al., 1985 and AMBROGI, 1990.

During 1986-1991 personnel from the Institute of Fisheries and Oceanology, Moscow, monitored benthic

communities m die Black Sea, near Sudak (PERELADOV el al., 1988). During this period benthic samples were

collected 2-4 times a year. Since P. caspersi was numerically dominant at the study site, die material was suitable

or an evaluation of seasonal and long-term changes in the population structure of this species.

Source :

BLACK SEA POPULATION OF PRIONOSPIO CASPERSI

165

MATERIALS AND METHODS

The study was carried out in Kapsel Bay, near the town of Sudak on die southeastern coast of the Crimean

Peninsula, in the area of a mussel (Mytilus galloprovincialis Lamarck, 1819) farm (Fig. 1). Benthic samples were

collected at the same stations twice a year in 1986-1987 and 1989-1991 (spring and late summer or autumn), and

once every three months in 1988. Although not all stations were sampled each time, all sampling periods except

November 1990 included samples from within and outside the mussel beds, for die most part about half of each

(Table 1). At each station 1-4 samples were taken by a Petersen grab (0.025 m2). The samples were sieved

through 0.5 mm mesh and all P. caspersi were removed, fixed in a 4 % formalin solution and counted. For study

of size-frequency distribution, specimens collected in February, April and August 1988 were used. For each

specimen die surface area of die first 10 setigers was calculated according to die method of Ambrogi ei al. ( 1985).

The material is deposited in the A.N. Severtzov Institute of Evolutionary Animal Morphology and Ecology.

Russian Academy of Sciences, Moscow.

RESULTS

Prionospio caspersi inhabited clean fine sand and silty sand at depths of 9 to 23 m in the community of the

bivalve mollusc Chamelea gallina (L., 1758). At sites where the silty fraction prevailed, P. caspersi was absent. It

was not found at depths greater than 23 m which may have been the results of die predominance of silly sediments

here.

Size- frequency distribution of individuals based on the surface area of die first 10 sedgers is shown in Fig. 2.

The curves were unimodal in February and April and bimodal in August. The modal area of the first 10 setigers

was 0.56 min2 (average: 0.62 mm2, n = 128 specimens) in February, increasing to 0.71 mm2 (average: 0.76 mm2,

n = 146) by April. The first peak of the size-frequency curve in August was formed by individuals with a modal

area of 0.34 mm2. This peak reflected the appearance of a new generation. The second peak was formed by

specimens with a modal area of 0.64-0.71 mm2. This corresponded to die single peak in winter and spring months

formed by specimens of the previous generation. The period from April to August was characterized by negative

growdi of die population probably reflecting the death of die parent population.

No. of specimens

“* February April August

N-128 Nr146 N -84

FlG. 2. - Prionospio caspersi. Size- frequency curves based on surface area of anterior end calculated according to method of

Ambrogi et a/. (1985). Arrow indicates appearance of recruits.

166

A. B RITA YE V. A. CASTELLI & T. S. AKS1UK

FIG. 3. Prionospio caspersi. Seasonal and long-term changes in population density in Kapsel Bay. Black Sea. Arrow

indicates last find of this species.

Prionospio caspersi outstripped other benthic species in terms of density and frequency of occurrence in 1986-

1988. The maximum density was about 2440 ind.m?, and the mean density varied from 96 to 730 ind. m2.

Table 1. — Prionospio caspersi. Frequency of occurrence at 1 1 stations (A-K) in Kapseh Bay, die Black Sea.

Source MNHN. Paris

BLACK SEA POPULATION OF PRIONOSPIO CASPERS!

167

In 1988, hcniliic samples were collected in all seasons, so diis year is more suitable than die others for an

analysis of the seasonal dynamics of the population. Population density was maximal in winter and spring,

decreasing in summer and increasing in autumn (Fig. 3). A decrease of population density in summer was noted

also in 1986 and 1987. The decrease in population density in August-September was accompanied by a reduced

frequency of occurrence (Table 1 ).

As a result of benthic community monitoring from 1986 to 1991, the population of P. caspersi population may

be followed until April 1989 when it was taken for die last time (Fig. 3). P. caspersi was absent from samples

taken in September 1989 through 1991.

DISCUSSION

The size- frequency histograms suggest that a recruitment took place in die second part of die summer. These

data agree with AMBROGl's (1990) observations. He found diat P. caspersi had an annual life cycle widi intensive

recruiunent in die beginning of July in die Adriatic Sea. The decrease in density and frequency of occurrence in

August-September was probably related with the change of generations. High mortality eliminated the parent

population, and at die same time die density of die new generation was low as a result of die prolonged period of

recruitment which was not yet over.

The population density of P. caspersi in die Adriadc Sea (Ambrogi, 1990) was about 15-20 times higher than

in the Black Sea. The trophic conditions in diesc areas are similar. The concentration of organic carbon in the

Black Sea varied from 4.5 to 8.1 gC.kg1 in winter and summer, respectively (Pereladov, pers. comm.). This is

similar to die values found in die Adriatic Sea by Ambrogi (1990) (2. 1-8.2 gC.kg-i). The sediment structure was

similar at both sites. However, die hydrodynamic conditions in the two areas were different. AMBROGI (1990)

emphasized the stability of environmental parameters in die Adriatic. In contrast, Kapsel Bay is an exposed bay

and die upper layer of sediment is influenced by wave action to 15-20 m, the lower depth of die distribution of P.

caspersi. This species inhabits the thin upper layer of sediments and is usually disturbed during storms. Therefore!

wave action is probably die main factor causing a decrease in the density of P. caspersi on die southeastern coast

of Crimea.

This theory provides an explanation for the disappearance of P. caspersi in the atituinn of 1989. In early

September 1989 a storm preceded the disappearance of P. caspersi (Pereladov, pers. comm.). In this period the

entire population was essentially comprised of young specimens. Destruction of the P. caspersi population was

probably due to the co-occurrence of this storm with the most vulnerable period of the life cycle. The absence of

recruitment in 1990-1991 probably reflected the absence of drift larvae from adjacent areas, i.e., die disappearance

of P. caspersi in adjacent areas.

ACKNOWLEDGEMENTS

We are grateful to Mr. M.V. Pereladov for organizing the monitoring of benthic communities in Kapsel Bay

and for fruitful discussion of this paper. We gratefully acknowledge our colleagues Dr. E.G. Zavarzina, Mrs.

N.V. Britayeva and Mr. M.A. Saburin for their assistance in collecting and sorting material. We thank Dr. Y.I.

Kantor and Dr. J.A. CHERNIAEV for help with the English and French translations, respectively. We are grateful

to Dr. M.E. Petersen, whose thoughtful comments improved this manuscript.

REFERENCES

AMBROGI. R.. 1990. — Secondary production of Prionospio caspersi (Annelida: Polychaeta: Spionidae). Mar. Biol.. 104 : 437-

442.

Ambrogi. R., Fontana, P.. & Occhipinti Ambrogi, A., 1985. Un metodo planimetrico per biometrie di invertebrati

marini. Studio preliminare di una popolazione di anellidi policheli. Nova Thalassia. 7 (suppl. 3) : 269-274.

Britayev, T.A.. CASTELLI, A., & AKSIUK. T.S., 1991. — On the finding of Prionospio caspersi (Polychaeta, Spionidae) in the

Black Sea. Zool. Zh., 70 : 5-9 (In Russian, English summary).

168

A. BRITAYEV, A. CASTELLI & T. S. AKSIUK

Gu£RIN, J.-P.. 1970. — Description dcs stades larvaires de Prionospio caspersi Laubier (Annelide polychete). Repartition dcs

larves de Prionospio en Mediterranee Occidentale. Tethys , 2 : 35-40.

Lardicci. C. 1989. Censimento dei policheti dei mari italiani. Spionidae Grubc, 1850. Atti Soc. Tosc. Sci. Nat., Mem., Serie

B, 96: 121-152.

Laubier. L., 1962. — Quelques Annclidcs polychetes de la lagune dc Venise, description de Prionospio caspersi n. sp. Vie <&

Milieu, 13 : 124-159.

Laubier. L.. 1965. Quelques Annelides polychetes de 1’Atlantique reccmment signalees ou nouvellcs en Mediterranee

occidentale. Rapp. P.V. Comm. Ini. Mer Medit. , 18 : 135-138.

Pereladov, M.V., Britayev. T.A., Zavarzina, E.G.. & Aksiuk, T.S., 1988. — The influence of mussel farming on the

benthic communities of Sudak Bay (the Black Sea). Ribnoe Hozaistvo . 9 : 27-30 (In Russian).

Source : MNHN, Paris

18

Systematics, ecology and biogeographical relationships in

the sub-family Travisiinae (Polychaeta, Opheliidae)

Jean-Claude DAUVIN* & Gerard BELLAN**

♦Laboratoire de Biologic des Invertebres Marins et Malacologie, URA CNRS 699

57 rue Cuvier, 7523 1 Paris Cedex 05. France

♦♦Centre Oceanologique de Marseille, URA CNRS 041

Station Marine d’Endoume, rue de la Battcrie des Lions, 13007 Marseille, France

ABSTRACT

The Opheliidae is divided into three monophyletic groups corresponding to the three sub-families defined by HARTMANN-

SchrOder: Ophelininae, Opheliinae and Travisiinae. 'Ihe object of the current paper is to offer a contribution to the knowledge

of the sub-family Travisiinae including taxonomy, ecology, biogeographical distribution. Three genera are studied:

Dindymenides, Kesun and Travisia. Based on previous phenetic and phylogenetic studies of the family and sub-families, we

propose to consider Travisia as the only valid genus in the sub-family. Twenty-seven species and three sub-species are

recognized in this genus. However, many of them are incompletely described and the characters used in species-recognition

varies from one author to the next and the validity on some characters has not been recognized until recently. Most of the

species must be redefined based on recent findings; we are, however, able to propose a preliminary key to species. Species of

Travisia general inhabit a muddy substratum, from the intertidal to abyssal depths (7,800 m). Twenty-one taxa are found on the

continental shelf and 14 of these are limited to shelf depths (< 200 m). Eleven taxa are found at depths below 2,500 m; three

are strictly abyssal. The genus shows a world-wide distribution, but is especially well represented in the Pacific Ocean (21

taxa). Seven taxa are found in the Antarctic Ocean and 10 in the Atlantic Ocean. Sixteen taxa are exclusively to the Pacific

Ocean. Eight species with a large geographical range also show extended bathymetric ranges: T. glandulosa, T. J'orbesi. T.

fusus. T. gravieri, T. japonica, T kerguelensis, T. olens, and T. profundi. A study of the relationship between species and

biogeographical distribution is given.

RESUME

Systeniatique, ecologie et relations biogeographiques dans la sous-famille des Travisiinae (Polychetes, Opheliidae)

L ensemble des donntSes sur la famille des Opheliidae a etc reuni afin de fournir un etat actuel des connaissanccs sur cette

famille. Les Opheliidae se divisent en trois groupcs monophyletiques correspondant aux trois sous-famille decrites par

HARTMANN -SCHRODER : Ophelininae, Opheliinae et Travisiinae. L’objectif de cette note est de fournir une revue des

connaissanccs sur la taxonomie, lecologic, la distribution biogeographique de la sous-famille des Travisiinae. A partir de

considerations pheneliques et phylogeneliques, il est propose de reunir les trois genres decrits : Dindymenides, Kesun et

Travisia, dans le seul genre Travisia. Vingt-sept especes et trois sous-especes peuvent etre reconnues comme valides,

cependant beaucoup d’especes demeurent incompletement decrites el les caracteres morphologiques utilises changent d’un

DAUVIN. J.C. & G. BELLAN, 1994. Systematics, ecology and biogeographical relationships in the family Travisiinae

(Polychaeta, Ophelidae). In: J.-C. Dauvin, L. LAUBIER & D.J. RE1SH (Eds), Actes de la 4eme Conference intemationale des

Polychetes. Mdm. Mus. natn. Hist, nat., 162 : 169-184. Paris ISBN 2-85653-214-4.

Source : MNHN. Paris

170

J.C. DAUVIN & G. BELLAN

auteur & I'autre. Bien que la plupart des especes merite de nouvelles observations, il est propose une cle preliminaire

d'identification dcs especes du genre Travisia. Le genre est typique des substrats vaseux, il est rencontnS depuis la zone

intertidale jusqu'aux abysses (7800 in). Vingt-et-un taxons sont connus du plateau continental, 14 ne depassant pas cc plateau.

Onze taxons ont ete recenses a des profondeurs inferieures a 2500 in, trois d’entre eux sont strictement abyssaux. Le genre a

une distribution cosmopolite, mais il est particulierement bien represent^ dans l'oc^an Pacifique (21 taxons). Sept taxons sont

antarctiques. 11 atlantiques, 16 sont exclusifs clu Pacifique. Huit especes ont une large distribution geographique et

bathymetrique : T. glandulosa, T. forbesi, T. fusus, T. gravieri, I japonica. T. kerguelensis, T. olens, et T. profundi. Les

relations biogeographiques entre les especes ont ete recherchees.

INTRODUCTION

During the course of our research, we have had the opportunity to study the species belonging to family

Opheliidae, including die genus Ophelia (Bellan & Dauvin, 1991; Bellan-Santini et al ., 1992), and die family

in general (Bellan et al ., 1990). In diis last paper, die 12 genera of the family were analyzed to attempt a

coherent classification of the family. Our results confirm the subdivision into diree sub-families originally

proposed by Hartmann-Schroder (1971): Ophelininae, Opheliinae and Travisiinae. This last sub-family seems

particulary suitable to be studied because of die small number of accepted genera: Dindymenides , Kesun and

Travisia , its plesiomorphy, and its undespread ecological and geographical distributions. Neverdicless, one of die

difficulties lies in the incomplete description of many species, and the non-existence of type specimens. The lack

of accuracy of descriptions is due, usually, to age of the specimens, and the small number of specimens described,

but it is also necessary to point out the difficulties inherent to the morphological criteria used for these

descriptions. Our major objectives are to present the various problems remaining widiin the sub-family

Travisiinae, to present die state of die knowledge on this sub-family widi a preliminary key, to discuss the

generally admitted viewpoints, and to propose a certain number of interpretations and hypothesis as a basis for

future work.

TAXONOMIC STATUS OF GFNERA AND SPECIES OF TRAVISIINAE

The sub-family Travisiinae may be defined as following:

Opheliidae with short and grublike body, without lateral and ventral grooves or widi very reduced grooves.

Branchiae generally present, posterior setigers generally with epipodial pads. Anal cylinder usually short,

sometimes furrowed, anal cirri short, and diick setae smoodi or finely spinose.

The genus Travisia was first described by JOHNSTON (1840) as:

Diagnosis: Body short, fusiform or grublike, without distinct groove. Prostomium small, cone-shaped, two

nuchal organs. Branchiae present, lateral eyes absent: posterior epipodial pads more or less developed. Parapodial

small, without presetal lobes. Lateral sense organs present between parapodial rami. Anal cirri usually short and

thick. Setae simple, capillary, or hispid. First setiger appears before the mouth.

Two other genera have been described: Dindymene Kinberg, 1866, and Kesun Chamberlin 1919.

Diagnosis: Dindymene Kinberg, 1866 " Corpus fusiforme, segmenta 3-2 annulata, lobus cephalicus minutus,

lerminalis, nudus; segmenta buccalia tria, primum nudum; os inferum, transversum; pharynx sine papillis et

maxillis; pedes duplices, distantes, setis capillaribus: aliis laevibus, aliis serrulato-ciliatis; branchiae cirrosac,

usque a segmento buccali secundo; segmenta posteriora tuberculis binis utrinque praedita".

Chamberlin (1919) renamed this genus Dindymenides since die original name has been used in 1847 for a

Crustacean. He does not give more details on die diagnosis of the genus.

Bellan etal. (1990), following Fauchald (1977), kept Dindymenides as a valid genus on die basis of a

strong auloapomorphy: die serratulate-ciliale setae. However, these audiors pointed out that these characters

needed to be confirmed. A certain number of Travisiinae belonging to genus Kesun and Travisia have been also

described with hispid and/or scrratulated setae. Hartman (1948), who examined die Kinbcrg's material, did not

mention diese ornamentations. If we consider the position of the first setae with regard to die moudi, Hartman

stated diat die prostomium of die preserved specimen had been unnaturally flattened in a vial, resulting in the

misinterpretation of die anterior part of die animal. Hartman staled: "the first setae arc in front of the oral

aperture". Considering the wide variations of die body of die Travisiinae due to dieir conservation, we accept die

opinion of Hartman at least until we are in position to examine freshly material. Dindymene and thus also

Dindymenides is known only from a single record (Day, 1967). In summary, we prefer to consider diis genus

SYSTEM ATICS, ECOLOGY, BIOGEOGRAPHY IN TRAVISIINAE

171

invalid, following the opinion of Hartman (1948), and more recently Fauchald (in litt.). The only species

known in the genus, originally described as Dindymene concinna, must now be known as Travisia concinna

(KlNBERG, 1866).

Diagnosis: Kesun Chamberlin, 1919. "Body short, pointed at both ends, fusiform or grub-like. Body rounded

cylindrically, without ventral groove. Somites of the middle region triannulate, the others may be only biannulate

or entire. Prostomium small, wholly smooth and rounded, without processes. Parapodial tubercles small and

smooth, or wholly absent. No cirri or branchia on any somite. No eyes. With a series of lateral sensory pits as in

Travisia . Pygidium small, cylindrical, longitudinally furrowed. Segments not numerous (twenty-eight in the

type)".

Kesun was created by CHAMBERLIN(1919) for a species Kesun fusus distinguishable from the other species of

Travisia described at dial time, by the lack of "cirri" which are commonly interpreted as branchiae. Another

feature is the absence of epipodial pads on the last segments and the presence of an anal cylinder. Accepting for

the moment the absence of branchiae as a characteristic feature of the genus Kesun , we have to point out dial other

features mendoned, such as die anal cylinder and die lack of epipodial pads in the last setigers are not unique to

abrianchiate members of die sub-family. The anal cylinder of K. fusus is very short and not really distinguishable

from diat of Travisia profundi and from many odier species of the genus. The absence of epipodial pads is also

not a unique feature either. This leaves only one unequivoqual difference between Travisia and Kesun : die

absence of branchiae in die latter. In a previous paper, BELLAN et al (1990) argued diat this character should not

be used at a generic level. The fact diat members of Kesun are limited to badiyo-abyssal depdis might be used as a

characteristic feature; however this present lime, we propose to discard Kesun and retain only a single genus,

Travisia. Hartman (1965a) had already proposed this synonymy. The definition of die genus corresponding to

diat of the sub-family Travisiinae widi a supplementary character: die presence of pustulae or similar structure on

the body.

The fact that remains only one genus Travisia in die Travisiinae should not change die status of this sub¬

family. In Bellan el al. (1990), die classification of the Opheliidae family was made using sequencing which

means dial the first taxa (Travisiinae) is die sister group of till following groups with a rooted tree by a theoric

ancestor (see Willey, 1981). This classification taking into account the level of apparition in the cladogram was:

Family Opheliidae

Sub-family Travisiinae

Sub-family Opheliinae

Sub-family Ophelininae

This classification regards die very strong differenciation between die Travisiinae and the group Opheliinae +

Ophelininae, and respect the classical use of die three sub-families. In die present slate of the knowledge, it is not

possible to state on the filiation between die Opheliinae and Ophelininae.

ANALYSES OF TRAVISIINAE SPECIES

We have observed available types or specimens from 21 taxa. The examined specimens come from: 1) Natural

History Museum, London, 2) Smithsonian Institution, Washington, 3) Museum National d'Histoire Naturelle and

4) National History Museum of Los Angeles County. The numbers at the end of diese 21 species refer to the

museum where dicy are deposited. A lack of a number indicates that we did not see the specimen. Twenty-seven

species and diree sub-species are now retained. The alphabetical list of these taxa widi indication of the most

complete description available, die list of authors having cited the species, and dieir known geographical

distribution is given below:

• T. antarctica Hartman, 1967, pp. 139-140; Hartman, 1978. South Georgia, Antarctic, South Atlantic Ocean;

2,452-2,727 m. (2)

• T. arborifera Fauvel, 1932, pp. 191-193, fig. 33; Fauvel, 1953. Andaman sea, Gulf of Bengal; British Natural

History Museum Collection, 1 ex. off Burma coast, 35 m. Indian Ocean. 7-100 m. (1)

• T. brevis Moore, 1923, pp. 220-221; Berkeley & Berkeley, 1952, pp. 90-91, fig. 183; Banse &

Hobson, 1968; Hartman, 1969, pp. 343-344, 1 fig. Berkeley & Berkeley, 1942; Imajima, 1961, 1963, 1964;

Reish, 1965; Hartman, 1961, 1965b, 1969; Fauchald, 1972; Loi, 1980 ; Hobson, & Banse, 1981; Fauchald

& Hancock, 1981. Southern California, North-eastern Pacific, Bering Sea, Okhotsk Sea. 18-2,900 m. (2)

• T. carnea Verrill, 1873, pp. 508 & 604; EHLERS, 1887; PETTIBONE, 1954, pp. 296-298; Appy et al ., 1980.

According to Hobson & Banse, 1981, the designation of T. carnea by Berkeley, 1966, 1968 for British

172

J.C. DAUVIN & G. BELLAN

Columbia is incorrect; it is probably T. pupa. We have seen the holotype of T. parva Day, 1973 (p. 94, fig. 13), off

Beaufort, North Carolina. It has: 20 scligers, a posterior asetigerous segment, 19 pairs of branchiae, neither

parapodial lappets nor lateral crenulations. These characters are very similar of those of T. carnea Verrill, 1873,

and it is surprising that Day didn't compare his species with the Verrill's species which are found in the same area

and depth. We consider T. parva as a synonym of T. carnea. North-western Atlantic, Massachussets to long

Island, Arctic Alaska. 5-35 m. (2)

• T. chiloensis Kiikenthal, 1887, pp. 364-365, figs 1-3. Chiloe, South-eastern Pacific.

• T. c/iinensis Grube, 1869, p. 66; Augener, 1922, pp. 38-40. China Sea, North-western Pacific.

• T. concinna (Kinberg, 1866), p. 256; Kinberg, 1910, p. 66, plate 25, fig. 5; Hartman, 1948, pp. 113-1 14.

Algoa Bay, South Africa, 5-20 m.

• T. doellojuradoi Rioja, 1944, pp. 135-136, figs 57-59; Rioja, 1946. Argentina coasts, South-western Atlantic.

115 m.

• T. elongata Grube, 1866, p. 66; EHLERS, 1901, p. 171, plate 22, figs 11-14. AUGENER, 1922, p. 34. Iquique,

Perou, South-eastern Pacific.

• T.foetida Hartman, 1969, pp. 344-345, three figures; Fauchald, 1972, pp. 237-238, plate 49, fig. d; Fauchald

& Hancock, 1981; Moore, 1923, Hartman, 1963, 1965b, 1966a as T. pupa. Redondo Canyon, California,

North-eastern Pacific. 250-3,100 m. (4)

• T. forbesii Johnston, 1840, pp. 373-374, plate 19, figs 11-18; Rathke, 1843, pp. 192-194, plate 10, figs 9-12. de

Saint Joseph, 1898; McIntosh, 1908a, b; Fauvel, 1914, 1925; Annekova, 1937, 1938; Berkeley &

Berkeley, 1942; Stop-Bowitz, 1945, 1948; Wesenberg-Lund, 1950, 1951; Pettibone, 1956; Chlebovitsch,

1961; Day, 1961, 1967; Eliason, 1962; Hartman, 1965a; Hamond, 1966; Cabioch et al., 1968; RetiEre,

1968; GlEmarec, 1969; Kirkegaard. 1969; AMOUREUX, 1971; Levenstein, 1966, 1971/72; WOLFE, 1973;

Averincev, 1977; Holthe, 1977; Hobson, & Banse, 1981. According to Stop-Bowitz (1948) and as Eulers

(1897), the designation of T. forbesii from the coasts of Chile and Antarctic is doubtful. T. forbesii is characteristic

of the northern hemisphere where it is collected to 300 m (Levenstein, 1971/72). One specimen of T.forbesi

with 28 setigers from False Bay, South Africa, is in the collection of die Natural History Museum of London. We

confirm the presence of the species in South Africa. Arctic, Circumpolar: Novaya Zemlya, Davis Strait,

Spitsbergen, Kara sea, Alaska and Canadian Arctic, North-east America, Siberia, Bering sea to Washington

Sound. North Japan Sea, West and east Greenland, Iceland, Faroes, Norway. North sea, western Baltic, Great

Britain, France: off the mouth of the Amazonc, Brazil, South Africa. 0-3,000 m. (1, 3)

• T. forbesii intermedia (Annenkova, 1937), p. 177; Uschakov, 1955; Buzhinskaya, 1985. According to

Buzhinskaya (1985), we have considered T. kerguelensis McIntosh subsp. intermedia Annekova, 1937 as a T.

forbesi subsp. intermedia (Annekova, 1937). Japon Sea, North-western Pacific. 30 m to abyssal.

• T. fusiformis Kudenov, 1975, pp. 215-218, figs 17-23. Gulf of California. Mexico, North-eastern Pacific.

Intertidal. (4)

• T. fusus (Chamberlin, 1919), p. 386. plate 67, fig. 5 and plate 68, figs 1-2; LEVENSTEIN, 1970, 1971/72. Pacific

Ocean. 3,000-7,580 m. (2)

• T. gigas Hartman, 1938, p. 103, figs 46-48; Hartman, 1961, 1963; Berkeley & Berkeley, 1941, 1962;

BERKELEY, 1968; Reish, 1968: Hobson & Banse, 1981. California, North-eastern Pacific. 0-180 m. (2)

• T. glandulosa McIntosh, 1879, p. 506, figs. 15-16. We have seen the only known specimen of T. glandulosa. It

was found in North-western Atlantic at 3,300 in. It has: 7 mm length, no visible branchiae, a very distinct lateral

groove at the last setigers, pustulae in a row by annulus. These characters are very similar to those of Kesun

abyssorum Monro, 1930. Even if T. glandulosa was rather poorly described by MdNTOSH, it does not seem that

Monro compare his specimen with McIntosh's species. Considering the similarity of Kesun abyssorum Monro,

1930 with Travisia glandulosa McIntosh, 1879, we propose the synonymy of the two species. Monro, 1930, p.

167, fig. 69 8 8; Kirkegaard. 1956, p.71, fig. 10; Hartman, 1966b, p. 51: Monro, 1939; Augener, 1932;

Hartman, 1967; Levenstein, 1961a, 1961c, 1971/72, 1975, 1978; Averincev, 1974; Rozbaczylo, 1985.

Pacific Ocean, Antarctic Ocean, Atlantic Ocean. 193-6,850 m. ( 1)

• I granulata Moore, 1923. pp. 219-220; Hartman, 1938, 1961, 1969; Loi. 1980. Southern California, North¬

eastern Pacific. 45-105 m. (2)

• I gravieri (McIntosh, 1908a), pp. 383-384; McIntosh, 1915, pp 29-30, plate 95, fig. 8; Hartman, 1965a, pp.

191-192; Hartman & Fauchald, 1971: Levenstein, 1971/72; Amoureux, 1982; Kirkegaard, 1980. Atlantic

Ocean. 539-7,800 m. (1)

• T. hobsonae Santos, 1977, pp. 559-564, fig. 1; Uebelacker, 1984, pp. 17-4, 17-5, figs 17-1, 17-2. Gulf of

Mexico, North-western Atlantic. 10-110 m. (2)

Source :

SYSTEM ATICS. ECOLOGY. BIOGEOGRAPHY IN TRAVISHNAE

173

• 7. Iiorsti Caullery, 1944, pp. 47-48, fig. 40. Java Sea, Pacific. 959 m.

• 7. japonica Fujiwara, 1933, pp. 91-103, plate I, figs 1-8, plate II, figs. 1-6: Monro, 1934, pp. 373-374, fig. 8 as

T. chinensis Grube, 1869 according to Hartman, 1959; FAUVEL, 1936, pp. 75-78. Fauvel, 1933: USCHAKOV,

1955; Imajima & Hartman, 1964, Berkeley, 1966: Uchida. 1967; Hobson & Banse, 1981; Fournier &

LEVINGS, 1982: Buzhinskaya, 1985. Japan Sea, NorUi-western Pacific. 10-105 m. (1, 3)

• 7. kerguelensis McIntosh, 1885, pp. 357-359, plate 43, fig. 10, plate 36A, figs 1-2: Ehlers, 1897, pp. 97-98,

plate 6, figs. 159-161: Augf.ner. 1922, pp. 36-37; Hartman, 1966b, p. 54. plate 17, figs 4-5; Averincev, 1982

p. 34. plate 5. figs 12-14; EHLERS, 1901, 1908, 1912: AUGENER, 1923, 1932; MONRO, 1930, 1936, 1939; Fauveu

1941; Rioja, 1944, 1946; Hartman 1953. 1967, 1978: Knox, 1962; Averincev, 1974; Day & Hutchings,

1979; Rozbaczylo, 1985; Hartmann-Schroder, 1986; Hartmann-Schroder & Rosenfeldt, 1989.

Kerguelen, Southern Indian, Southern Atlantic, Antarctic Ocean. 0-1,837 m. (1, 3)

•7’. kerguelensis gravieri Monro, 1930, p. 167, fig. 68: Hartman, 1966b; Hartmann-SchrOder &

Rosenfeldt, 1989. Palmer Archipelo, Antarctic Ocean. 259-315 m. (1)

• 7. lilhopliila Kinberg, 1866, p. 256; Augener, 1922, pp. 32-33; Hartman, 1966b, p. 54, plate 17, figs 7-10.

HUTCHINGS & Murray, 1984, p. 79; Hartman, 1952. Australia, South-western Pacific. 20-180 m.

• T. nigrocincta (Ehlers, 1913), p. 525; Hartman, 1966b, 1967. South Pacific, Antarctic. 2,725 m.

• 7. olens Ehlers, 1897, p. 98-99, plate 6, figs 162-163; Augener, 1922, pp. 35-36; Ehlers, 1901, 1912; Monro,

1930: Augener, 1932; Benham, 1950; Hartman, 1966b. 1967; Day & Hutchings, 1979. Hartmann-

Schroder & Hartmann, 1980; Rozbaczylo, 1985. One ex. Discovery st 939, 08/18/1932, 35°49'6S-173°27'E,

87 m. The designation of 7. olens by Fauvel, 1943 from California was probably incorrect, Hartman, 1969 did

not cite the species from California. It may be T. granulate i. Cape Horn. Scotia Sea, South-western Atlantic,

Antarctic, New Zealand, South-eastern Pacific. 0-1,120 m. (i)

• 7 olens Ehlers novae zealandiae Benham, 1927, pp. 12.3-128, plate 2, figs 70-72. Ehlers. 1897, 1907, 1912 as

T olens ; Benham, 1950, Day & Hutchings, 1979. British Natural History Museum Collection: 9 ex. from

Portobello. South Island, New Zealand. New Zealand, South-western Pacific. 0-20 m. (1)

• 7. oregonensis Fauchald & Hancock. 1981, p. 19. Offshore Oregon, North-eastern Pacific. 1,600-1.800 m. (4)

• T. profundi Chamberlin, 1919, pp. 387-389. plate 67, figs 1-4; USCHAKOV, 1955; Kirkegaard, 1956;

LEVENSTEIN, 1960, 1961a. b, 1966, 1970, 1971/72, 1975, 1978: Hartman, 1967. Atlantic (Angola) and Pacific

Ocean (Mid Bassin), Antarctic Ocean. 975-7,290 m. (2)

• T. pupa Moore, 1906, pp. 228-230, plate 11, fig. 29; Treadwell, 1914; Uschakov, 1955; Lf.venstein, 1960,

1961b, 1966, 1971/72; Hartman, 1961; Berkeley, 1966, 1968: Berkeley & Berkeley, 1942, 1952; Hobson

& Banse, 1981. Nordi eastern Pacific. 33-3,012 m. (2)

DISCUSSION OF THE MORPHOLOGICAL CHARACTERS

The shared characters of all species of Travisia include the presence of nuchal organs and interramal sense

organs; the capillary setae are often hispid and all species lack eyes. Characters used to distinguish the species

include the presence of lobes or papillae on the pygidium, the position of the nephridiophores and the total

number of setigers present. Few characters are unique to a single taxon. The body-shape is more variable, more or

less fusiform or grub-shaped, but the shape may vary with the numbers of segments present and with the quality of

fixation. The prostomium is pointed in all species, except in 7. foetida, which is truncate. Lateral and mid-ventral

grooves are generally absent; the development of these grooves characterize die different sub-families, however

Uiey are present, but poorly developed in some taxa. For example, a short lateral groove is present in I

glandulosa and a mid-ventral one in 7. fusiformis, T. gravieri and T. hobsonae. Branchiae are present except in the

species being transferred from Kesun: 7. fusus, T. glandulosa, T. gravieri, and 7. nigrocincta. The branchiae are

cirriform except in T. arborifera which has branching branchiae. They are present from setiger 2, except in T.

hobsonae, sometimes in T. cornea, and T. profundi where they arc present from setiger 3. Unusual lobes or

papillae are present on (he pygidium in T. japonica, T. gigas, 7. kerguenlensis gravieri. Nephridiopores arc

present on setigers 3-14 except in T. brevis (7-25), T. chiloensis (7-14?), 7. japonica (1 1-14 in die original

description but 3-14 in Fauvel, 1933). The number (n) of setigers is relatively stable in a given species (n ± 5)

except in 7. granulata 32-50, 7. japonica 32-39 and 7. litltopliila 44-53. It would be interesting to study die actual

significance of diis variability as a possible character at die specific level.

A last point, is die variability of the degree of papillation in the posterior segments as described in 7.

kerguelensis by Monro (1930). Some difficulties remain in ascertaining the identity of four similar taxa, all

174

J.C. DAUVIN & G. BELL AN

described from southern oceans. They were distinguished on the number of segments and the papillation: T.

kerguelensis (23-27 segments), T. kerguelensis gravieri (25), T. olens (29-36), and T. olens novae zealandiae (38-

40).

PRELIMINARY KEY TO THE TRAVISIINAE

A preliminary key of the species Travisia is presented which is provisional due to the difficulties in correctly

interpreting die available descriptions, some of which are incomplete. The need of a phenetic and phylogenetic

study is necessary in order to test die validity of characters. Before, diis can be done, it is necessary to have a

complete redescription for all species. The following characters must be accurately described in all species:

- color and shape of live specimen;

- presence, shape, and variability of posterior lateral crenuladons and parapodial lappets;

- number and variability of number of segments and setigers;

- number of branchiae;

- distribution of pustulae on die body;

- shape of die pygidium and pygidial papillae.

1 Branchiae absent .

Branchiae present .

2 Lateral groove in the last 10 segments

Lateral groove absent .

3 Body grub-shaped, < 25 segments, mid-ventral groove present, very short setae . 7'. gravieri

Body fusiform, > 25 segments, fascicles of distinguished setae . 4

4 Segment number 28, > 25 setigers . T.fusus

Segment number 25, 17 setigers . 7- nigrocincta

5 Prostomium truncated, 31 setigers, large species . T.foetida

Prostomium pointed conical . 6

6 Branchiae branched . T. arborifera

Branchiae cirri form . 7

7 Mid- ventral groove present . 8

Mid-ventral groove absent . ®

8 Mid-ventral groove slightly developed, 30-31 setigers, parapodial lappets developed ..I hobsonae

Mid-ventral groove and parapodial lappets well developed, 34-35 setigers . T.fusiformis

9 Segment number > 40 . 10

Segment number <40 . 13

10 Posterior parapodia with lobes or lappets . 11

Posterior parapodia without lobes or lappets . 12

1 1 Posterior parapodia with triangular lappets, pygidium collarlike with 6 long

dorsal papillae, length about 10 cm . I gigas

Posterior parapodia with small lappets, knob pygidium, length about 3 cm . T. elongata

12 Epithelium with large, dorsal and ventral coarse pustules, setiger number to

about 45, pygidium with 12-13 irregular papillae . T. granulata

Epithelium finely reticulated, from 44 to 53 setigers, pygidium with 7 cirri . I lithophila

13 Segment number > 30 . 14

Segment number < 30 . 1 8

14 Posterior lappets absent, 26-45 setigers . T granulata

. 2

. 5

T. glandulosa

. . . 3

Source

SYSTEMATJCS, ECOLOGY. BIOGEOGRAPHY IN TRAVISDNAE

175

Posterior lappets and lateral crenulations developed . 15

15 Pygidium widi an oval ventral lobe and 6 laterodorsal palpi . 16

Pygidium shape otherwise . 17

16 Laterodorsal palpi well developed, segment number 32-39, 26-32 branchiae pairs T. japonica

Segment number 35, 33 pairs of branchiae . T. concinna

17 Segment number 29-32 . j 0[ens

Segment number 38-40 . j. olens novae

zealandia

18 Setigers number = 18, 23 segments . T. orogenensis

Setigers number > 20 . 19

19 Parapodial lappets reduced or absent . 20

Parapodial lappets present . 23

20 Setigers number > 20, 25-29 segments, pygidium small, longitudinally furrowed . I cornea

Setigers number > 25 . 21

21 Numbers of branchiae pairs 9-12, 26 setigers and 25-27 segments . I profundi

Numbers of branchiae > 15 . 22

22 Segments number 30-32, 25-28 setigers, 22-25 pairs of branchiae number . T. pupa

Segments number < 30, about 25 setigers, 17-21 pairs of branchiae, anal

cylinder surrounded by a circlet of short papillae . T antarctica

23 Body pigmented in red purple, 17 pairs of branchiae . T. doellojuradoi

Body not pigmented in red purple, > 18 pairs of branchiae . . . 24

24 2 posterior achaetous segments . 25

3-5 posterior achaetous segments . 28

25 Parapodial lappets well developed, posterior part of die body finishing truncated . 26

Parapodial lappets little developed, posterior part of the body tapered to die pygidium . 27

26 Lateral lappets well developed, pygidium cylindrical . T. kerguelensis

Laterals lappets absent a pair of dorsal anal cirri at die end of die anal cylinder . I kerguelensis gravieri

27 Sedgers number 23-26, posterior margin of abdominal segment smoodi,

not scalloped, pygidium ovoid . T. forbesii

Setigers number 26-29, posterior margin of abdominal ondulate or serrulate,

pygidium cylindrical . T. forbesii intermedia

28 Parapodial lappets Iitde developed, pygidial knob pigmented, 23 setigers,

28 segments . j horsti

Parapodial lappets developed, pygidium not pigmented . 29

29 Branchiae number > 20, 27 segments, 24 setigers . T. chiloensis

Branchiae number < 20, 29 segments . 30

30 Sedgers number 23-25 . T. brevis

Sedgers number 27 . T. chinensis

BIOGEOGRAPHICAL DISTRIBUTION

Table 1 summarizes available data of species distribution. Only two species occur in Arctic Ocean; Antarctic

Ocean is richer widi eight taxa. I antarctica is present in die far-south (Soudi Georgia) of die Atlantic Ocean. Ten

species are present in die Atlantic Ocean, two of which are restricted to die northern part, five to die soudiern part

176

J.C. DAUVIN & G. BE LI -AN

and three have an extended distribution. Twenty-one taxa are present in die Pacit.c Ocean, 13 are restricted to the

north with T arborifera found in the Gulf of Bengal which is the single species collected in the Indian Ocean. Six

species arc known to be only from the south Pacific Ocean. Eight species have a large biogeograph.cal

distribution: T. glandulosa. T. forbesi, T. Jusus, T. gravieri. T. japonic". T. kerguelensis. T. olens. and 7. profundi.

Table 1. — Biogeographical distribution of Travisia species from the world's oceans.

BATHYMETRIC DISTRIBUTION

Three species T. chiloensis, T. chinensis and T. elongata were described without indication of original depth,

and were probably littoral species. Among the odier 27 taxa, 16 are present in the bathyal and/or the abyssal

depths and 10 are exclusively badiyo-abyssal (Fig. 1). Eighteen species are found on die continental shelf among

which only five species are collected at depths less dian 100 m.

Source : MNHN. Paris

SYSTEM ATICS, ECOLOGY, BIOGEOGRAPHY IN TRAVISHNAE

177

Depth in m

100 1000 10 000

FIG. 1. — Bathymetric distribution of Travisia species from the world’s oceans.

Source : MNHN, Paris

178

J.C. DAUVIN & G. BELLAN

ECOLOGICAL AND BIOLOGICAL DISTRIBUTION

The data on the ecology of the species are rarely reported and therefore die ecological and biological data are

incomplete. Most of the deeper species are found in bathyal and abyssal mud. The littoral species are found

especially in muddy and fine sand. T. foetida inhabits essentially clean sands in low intertidal and in die upper part

of die subtidal. However, this species has been found also in many different types of soft-bottom subsuates. Due

to its widespread distribution bodi geographical and badiymetric, I forbesii appears to be ubiquitous. This

ubiquity may be the result of die presence of a complex of species. The principally northern species T.forbesi may

have a counterpart in the southern hemisphere widi T. kerguelensis and I olens and their sub-species.

Travisia are considered non-selective deposit-feeders. In the intertidal sand at Tampa Bay, Florida, specimens

of Travisia hobsonae had only sand particles in dieir gut widi no particles finer than 100 pm ; grains as large as

475 pm were removed with a median size of 230 pm (Dauer, 1980). The low level of food specialization in

adults contrasts sharply widi die high level of precision in the selection of substrata by juveniles (RETitRE, 1971,

1972).

Travisia forbesi lives 3.5 years at Dinard (English Channel); die spawning occurs at die end of die autumn and

during die winter; development is direct without larval dispersion (RETlfeRE, 1971, 1972). T. hobsonae reproduces

the year round in Tampa Bay (DAUER, 1980); its densities could reach an annual average of 1,100 nr2 at certain

stations.

DISCUSSION

This paper is a first step toward the study of Travisiinae and to die knowledge of the Opheliidae family. The

sub-family Travisiinae is die most plesiomorph (BELLAN et al., 1990) and is well defined in relation to the two

odier sub-families. This paper proposes to bring together all the species of this sub-family into the one genus

Travisia Johnston, 1840. The examination of available types has allowed us to place into synonymy Kesun

abyssorum Monro, 1930 with Travisia glandulosa McIntosh, 1879, and T. parva Day, 1973 widi T carnea

Verrill, 1873. Five species T. chiloensis, T. chinensis, T. concinna, T. elongata and T. horsti which have not (or

rarely) been found since dieir descripdon, remain doubtful and must be re-examined. Many characters should be

used in defining each species: color and shape of live specimens; presence, shape, and variability of posterior

lateral crenulations and parapodial lappets; number and variability of number of segments and setigers; number of

branchiae; distribution of pustulae on die body; shape of die pygidium and pygidial papillae. The variability of die

number of setigers, segments, and branchiae must be defined using a large number of specimens of each species.

This work would allowed in a further step to study the phenetic and the phylogenetic relationship between the

species. However, genetical studies must be established: 1) the real extended distribution of T. forbesii and

T. forbesii intermedia (nordiern species) ; 1\ forbesii may be a complex widi slight morphological differences; 2)

the genetical distance and variability of die southern species and their sub-species: T. kerguelensis, T. kerguelensis

gravieri, T olens and T. olens novae zealandiae. These four taxa are distinguishable essentially by die number of

segments and setigers, so they show a continuum between T. kerguelensis widi a number of segments which could

be reduced to 23 and T. olens novae zealandiae which a number of segments reaching 40. T. kerguelensis is

known to show a great variability of papillaUon in the posterior segments (MONRO, 1930).

It is clear diat the data on ecological and biological features are insufficient. Biological data are limited to T.

forbesii and T. hobsonae . Such studies must be extended to other species and populations. In the past few years

several works on Ophelia , such as diose of Riser (1987) and Harris (1991) have demonstrated that biological

(type of development) and ecological data (habitat) could be good criteria to ascertain on the validity of a

particular species in this family.

Travisia is typically a deep water Pacific genus. Badiymetric distributions of Travisia and Ophelia (BELLAN &

Dauvin, 1991) show that Ophelia occurs preferentially in shallow waters and in the Atlantic whereas Travisia

species dominate in the bathyal and abyssal depdis in the Pacific. This indicates diat die speciation of these two

genera could be parallel. In Ampeliscidae (Amphipoda), another marine diversified family, Dauvin & Bellan-

Santini (1990) have also distinguished two distribution schemes widi Ampelisca in shallow water and Haploops

in continental and badiyal depths.

New data are need before elucidating die evolution of the genus. Future works and prospects on Travisia

genus, but also on other genera of Opheliidae may reveal correlations between species, phyletic, bathymetric and

biogeographic features.

Source :

SYSTEM ATICS. ECOLOGY. BIOGEOGR API 1Y IN TRAVISDNAE

179

ACKNOWLEDGEMENTS

1'lie authors would like lo thank their colleagues for lending types and specimens deposited in die collections.

Dr Alex MUIR, Natural History Museum, London, Drs K. Fauchald and L. Ward, Smithsonian Institution,

Washington, L.H. Harris, Natural History Museum of Los Angeles County, Dr Fauchald also for his remarks

on die Travisiinae. Dr Alex Muir was particularly hepl'ul during the visit in London of J.C. Dauvin, which was

made possible by a grant from the M.N.II.N. (Bonus Quality Recherche, Musdum 1991, M31). They also wish to

diank P. CiILLET for access to the library of the Cadiolic University of Angers, A.B. Davies, Emory Univ.,

Atlanta, GA, for her help in correcting die manuscript, and D. Reish and K. Fauchald for dieir very constructive

suggestions on die first draft.

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Source ;

19

A new Species of Ophryotrocha

(Polychaeta, Dorvilleidae) associated with Ice Scours

in the Canadian Arctic Archipelago

Judith A. FOURNIER & Kathleen E. CONLAN

Invertebrate Zoology. Collections and Research Division

Canadian Museum of Nature/M usee canadien de la nature.

C.P./P. O. Box 3443. Station/Succ. “D”

Ottawa. Ontario Canada. KIP 6P4

ABSTRACT

Ophryotrocha spatula sp. n. is described from ice scours off Cornwallis Island in the Canadian Arctic Archipelago. This

species resembles O. scarlatoi Averincev. 1989 in having the last 5-12 setigers laterally prolonged into a broad, lobulate flange

but dillers 1mm this species in the structure of the jaw apparatus and setae and in possessing ventral parapodial cirri and a

median anal cirrus.

RESUME

Une nouvclle espece d' Ophryotrocha (Polychcte, Dorvilleidae) associec aux sillons d'icebergs dans I'Archipel

arcti(|iie canadien

L.e polychcte Ophryotrocha spatula sp. n. en provenance dc sillons d'icebergs pres de Cornwallis Island dans I'Archipel

arctiquc canadien est decrit. Cette espece resscmble a O. scarlatoi Averincev 1989. par ses bords dorsaux des 5-12 setigercs

posterieurs elargis en forme de lobe membraneux, mais el le s'en distingue par les soies, la forme des machoires. et la presence

de cirres ventraux paiapodiaux et un ciire median anal.

INTRODUCTION

A joint Canadian/Unitcd Stales team has been studying scour formations caused by grounded multi-year ice

off the coast of Cornwallis Island, Northwest Territories in the Canadian Arctic Archipelago (Queen Elizabeth

Islands). Icescouring is probably the most disruptive and widespread physical disturbance to marine bottom

communities in polar waters. In the Arctic, pressure ridges of ice scour the sea floor to depths of 60 m and larger

icebergs ground as deep as 750 m (Lewis & Blasco, 1990). The team has been investigating the

FOURNIER. J. A. & K.E. CONLAN. 1994. — A New Species of Ophtyotrocha (Polychacia. Dorvilleidae) associated with Ice

Scours in the Canadian Arctic Archipelago. In: J.-C. DaUVIN. L. LaUBIER & D.J. REISH (Eds). Actes de la 4eme Conference

internationale des Polycheles. Mem. Mus. natn. Hist. nat.. 162 : 185-190. Paris ISBN 2-85653-214-4.

Source : MNHN. Paris

186

J. A. FOURNIER & K. E. CONLAN

benthic population and community responses to ice scour, documenting the successional stages of biotic recovery

in order to determine whether widespread patterns of zonation and larger spatial and temporal community mosaics

are correlated to the disturbance.

An undescribed dorvilleid of the genus Ophryotrocha was among the most abundant polychaete species and

showed a strong positive association with the disturbed sediments of the ice scours and berms. Mature specimens

of this species have the dorsal surface of die last 5-9 segments laterally prolonged into a lobulated spoon-shaped

flange. The species resembles Ophryotrocha scalatoi Averincev, 1989 from Franz-Joseph Land and Norway

(OUG, pers. comm.) but differs in details of jaw dentition and the presence of ventral parapodial cirri, most

noticeable in die posterior segments.

METHODS

Samples were collected by Hunter S. LENIHAN and Kathleen E. Conlan using diver-operated hand cores

pressed into the sediment. Six cores were collected from locations inside and outside each scour and from the

scour berm itself for a total of 18 samples from each of four scours. The 72 samples yielded a total of 551

specimens of the new species.

Samples were screened through a 0.5 mm mesh, fixed in 4 % formaldehyde solution and later transferred to

70 % ethanol. Final sorting was done in die laboratory under a dissection microscope. Specimens were examined

under dissection and phase-contrast compound microscopes. Drawings were done with a drawing tube. Ocular

micrometers in both compound and dissecting microscopes were used for measurements. Body width

measurements do not include parapodia.

DESCRIPTION OF COLLECTION SITES

Ice Scour 1 : Cape Martyr, Cornwallis Island, 74°4F N, 95°06' W, depdi 15 m; outside scour (one specimen),

scour berm (18 specimens), inside scour (27 specimens) sampled 31 July 1991. Outside of scour had gravel/cobble

substrate over silt, little Laminaria cover, exposed to frequent strong currents. Scour was perpendicular to

shoreline, 3-4 m wide, 1.5-2 m deep into sediment, more than 40 m long, estimated age less than one year,

probably produced during spring breakup of ice. Sediment inside scour loose and very soft, 4-5 cm oxic layer

covering grey anoxic zone. Scour berm with 7-8 mm oxic layer covering sediment. Epifauna outside scour

comprised very abundant echinoderms (ophiuroids, echinoids, asteroids, holothuroids), bivalves (Mya iruncata L.,

Serripes groenlandicus (Brugui£re), Astarte borealis (Schumacher)) and soft corals (Gersemia sp.).

Ice Scour 2: Assistance Bay, Cornwallis Island, 74°39' N, 94° 18' W, depth 7 m; outside (31 specimens), scour

berm (157 specimens) and inside (94 specimens) sampled 2 August 1991. Scour parallel to shore line in semi-

protected bay, well Hushed by strong currents and river flow. Scour estimated to have formed within previous 24

hours, about 6 m wide, 0.5 m deep and over 50 m long. Scour bottom hard with very little loose sediment over

large cobbles. Scour berm 5-10 cm high with stones and cobble. No epifauna visible within scour.

Ice Scour 3 : Resolute Bay, Cornwallis Island, 74°4F N, 94°50' W, depth 10 m; outside scour (zero specimens)

sampled August 4, 1991, scour berm (125 specimens) and inside (44 specimens) 8 August 1991. Circular "crater"

in area of 40-60 % Laminaria cover, estimated to have formed in previous 48 hours, more than 25 m in diameter,

0.25 m deep to hardpan. Berm 2-2.5 m high.

Ice Scour 4: Resolute Bay, Cornwallis Island, 74°41' N, 94°50' W, depth 7 m; outside (1 specimen) scour berm

(51 specimens), and inside (two specimens), 8 August 1991. Scour estimated to have formed within previous 48

hours, about 30 m long, 3 m wide, cut to hardpan, 0.25 m deep. Berm about 1 m high, loose sediment with stones

and gravel. Pockets of anoxic sediment along length of trough. Only a few Buccinum sp. seen within scour, Mya

spp. and Macoma spp. on berm.

Resolute Bay is protected by a sill at the entrance. Bottom was fine sediment and cobble, about 20 cm deep,

over a hardpan base that prevented bivalves such as Mya spp. and Serripes groenlandicus from burrowing deeper.

Scours 3 and 4 were in the central pan of the bay, close to shore, in an area of dense Laminaria cover.

Source :

NF.W SPECIES OF OPHRYOTROCHA FROM ARCTIC CANADIAN ARCHIPELAGO

187

SYSTEMATICS

Ophryotrocha spatula n. sp.

Material Examined. — Holotype: CMN A 1993-0046, mature specimen, 3.7 mm long, 0.5 mm wide anteriorly,

flange 0.8 mm across at widest point. Type Locality: Assistance Bay, Cornwallis Island. Ice Scour 2, Core 2, scour

berm, 7 m depth, collected 2 August 1991.

Paratypes: CMN A 1992-0 158, 79 specimens, remainder of sample from scour berm, core 2, Ice Scour 2

Assistance Bay, Cornwallis Island.

An additional 471 specimens have been found in the rest of the samples (Table 1).

05 mo

Fig. 1. — a. Ophryotrocha spatula sp. n., dorsal view, holotype. most setae omitted, b. Paratype, ventral view, posterior, c.

Paratype. anterior view of median parapodium. d. Posterior view of posterior parapodium. setae omitted except for ventral

simple seta. e. f. Long and short blades of compound falcigers. g. Ventral simple seta. h. Tip of simple seta.

188

J. A. FOUR NI HR & K. H. CON LAN

SPECIES DIAGNOSIS. — Medium-sized Ophryotrocha , 3.7 to 5.5 mm long for 25-43 setigcrs, anterior body width

about 0.5 mm, dorsum of posterior 5-12 segments laterally expanded into a lobulatc flange (Fig. la). Prostomium

with 1 pair each palps and antennae, ovate. Single pair of small eyes usually visible on posterior margin of

prostomium. Jaw apparatus (Fig. 2) darkly sclerotized. mandibles rod-like with toothed, bifid anterior margin,

forceps P-type. inner edge with one row of about 10 large teeth interspersed with smaller ones and secondary ridge

with many fine teeth. Free denticles seven pairs in two groups. Parapodia with both dorsal and ventral cirri, former

difficult to discern in anterior parapodia. Supra-acicular setae simple unidentate blades with very finely serrated

edges. Sub-acicular setae compound, unidentate blades with very finely serrated edges, varying in length by factor

of two. Pygidium flattened, anal cirri ovate, inserted ventrally. Anus ventral or terminal depending on state of

dilation, bearing mid-ventral papilla.

DESCRIPTION ofholotype. — Holotype (Fig. la) 3.7 mm long for 32 setigers, body width 0.5 mm anteriorly,

0.8 mm at widest point of posterior flange. Colour in alcohol off-white. Body sparsely ciliated but setigcrous

segments have extensive glandular regions covering dorsum.

Prostomium rounded, bearing two small ovate antennae dorsally and pair of ventral palps almost identical in

size and shape. Fycs not visible.

Fig. 2. — Ophryotrocha spatula sp. n., jaw apparatus from paratype. a. Mandibles, b. Forceps (base broken), c. d. c. First

group of free denticles, f. g. h. i. second group of free denticles.

Peristomium followed by achactous apparent first segment. Mouth parts (Fig. 2) darkly sclerotized. Forceps

and free denticles forming separate group. Mandibles (l;ig. 2a) partially protruding, rod-shaped with jagged bifid

Source : MNHN. Paris

Ni:w SPECIES OF OPHRYOTROCHA I ROM ARCTIC CANADIAN ARCHIPELAGO

189

leading edge and several unpaired, irregular protrusions along length of shaft. Forceps (Fig. 2b) P-type (IIilbig &

Blake, 1991) with single main tooth, inner edge with row of about 10 large teeth interspersed with at least 20

smaller ones, secondary median ridge bearing row of much finer teeth: main shaft darkly sclerotized but

surrounded by thin flange.

Free denticles, seven pairs arranged in two primary groups (Fig. 2c-i). Denticles closest to the forceps (Fig. 2c-

c) dark and strongly toothed; median member (Fig 2c) fang-shaped. Outer denticles (Fig. 2f-i) thin and broad with

numerous long slender teeth interspersed with several stouter ones.

Parapodia uniform in shape; setae vary only in number. Dorsal and ventral cirri ovate but latter very difficult to

distinguish in anterior setigers. Presctal lobe truncate. Dorsal postsetal lobe rounded; ventral, retractile lobe

triangular and supported by single simple seta that resembles secondary emergent acicula (Fig. lc-d). Aciculae

very long and stout, seated proximally against row of longitudinal muscle group. Supra-acicular setae simple,

unidentate flattened blades with very finely denticulate lower margin (Fig. 1, c-g-h). Second superior seta longer

than others. Subacicular setae compound falcigers with blades varying in length by factor of two. unidentate with

very finely denticulate border, almost identical to supra-acicular setae in size and form.

Setiger 1 with one supra-acicular seta, three compound falcigers and one subacicular simple ventral seta.

Following setigers with four supra-acicular setae, six compound falcigers and one ventral simple seta. Last setiger

with two simple supra-aciculars, two compound falcigers and one ventral seta. Large specimens have more setae

per bundle but pattern invariable.

Last 9 setigers expanded into broad, spatulate flange (Fig. la), free from dorsal cirri which project freely from

below flange. (Fig. Ih).

Pygidium flattened with two ovate anal cirri inserted ventrally (Fig. lb). Anus ventral with opening occupying

ventral surface of last three setigers; stout ventral median papilla.

OTHER SPECIMENS. — Mature specimens reach 5.5 mm with 25 to 43 setigers. No direct linear relationship found

between body length and number ol setigers. Many specimens with adhering sand grains and fine clay particles.

While all were oil -white in colour, a few of the largest specimens had yellowish-brown tinge. Most specimens

have single pair of small eyes on posterior margin of the prostomium, usually covered by part of peristomium.

Posterior flange often curled dorsally, forming a cylinder. Some of largest specimens show little expansion, other

smaller ones, such as the holotype, almost double body width. Not all specimens have anal opening as extended as

holotype; it is sometimes contricted and terminal as illustrated in Figure lb.

No gametes found in the holotype or any of the other specimens examined, including the largest. A few

juveniles, about 2 mm long for 20 setigers, are present in the samples but all appear to be damaged. The jaw

apparatus shows obvious similarities to the adults but the posterior flange is not developed. Instead, the body

appears to terminate in an undifferentiated, asetigerous region. These specimens need more study.

Etymology. — The species name spatula is Latin for spoon ;uid refers to the diagnostic unique structure of die

posterior segments.

Comparison to other species of Ophryothrocha. — The extensive review of I Iilbig & Blake ( 199 1 ) provided

a table of characters of most of the known species in the genus but overlooked 0. scarlatoi Averincev, 1989 which

also has a broad posterior flange. This species was only superficially described and figured. Oug (in prep.) has

discovered several specimens from Norway that resemble 0. scarlatoi. These differ from the present specimens in

having longer mandibles, in details of the maxillae and setae, and in lacking ventral parapodial cirri and a median

anal papilla. It will be necessary to re-examine the types of O. scarlatoi in order to determine whether we are

dealing with one, two or three species or subspecies. Attempts to borrow the type specimens of O. scarlatoi have

been unsuccessful (E. OUG, pers. comm.).

The parapodia and setae of 0. spatula resemble those of 0. puerilis siberti (McIntosh, 1885) as illustrated by

GEORGE & Hartmann-Schroder and Hartmann-Schroder (1985). The parapodia are not as strongly lobed as

those of 0. lobifera Oug, 1978 but that species also has Upuerilis- type” setae. Although IIilbig & Blake (1991)

do not tabulate the presence/absence of anal cirri and papillae, there are species which lack anal cirri ( 0 .

paralabidion IIilbig & Blake, 1991; 0. sp. near scarlatoi Oug), species with cirri reduced to “thread-like”

appendages (0. bacci Parenti, 1961; 0. geryonicola (Esmark, 1874), species with the anus dorsal ( 0 . lobifera

Oug, 1978), and species with a ventral papilla as well as anal cirri (0. longidentata Josephson, 1975; 0. maculata

Akesson, 1973; 0. minuta Levi, 1954; 0. puerilis siberti (McIntosh, 1885)). It is possible that the presence of a

ventral papilla has been overlooked in other species.

190

J. A. FOURNIER & K. E. CONLAN

Fable 1 . — Distribution of Ophryotrocha spatula sp. n., pooled totals of six samples each collected from outside,

the berm and inside four different ice scours off Cornwallis Island, Canadian Arctic Archipelago.

DISTRIBUTION

Ophryotrocha spatula sp.n. is known only from the shallow waters of Barrow Strait off Cornwallis Island. It

shows a strong affinity for the disturbed sediments of ice scour berms or troughs as opposed to the compacted

sediment outside die scour (Table 1 ). It was much more abundant on fresh scours (2, 3, and 4) than the older scour

(1). Analysis of distribution against grain size (mean 0) failed to demonstrate a significant relationship (C = 0.255).

ACKNOWLEDGEMENTS

The authors arc grateful to Diana LAUBITZ, Collection Manager, Invertebrate Zoology for facilitating our

collaboration on diis project and for her constructive criticism of die manuscript. We thank Hunter LlNIHAN,

Brenda Konar, and staff of Moss Landing Marine Laboratories, California, and Buster Welch of die Department

of Fisheries and Oceans, Resolute Marine Laboratory for assistance in the field and laboratory Ed IlENDRYKS

helped widi specimen sorting. Francois GfiNIER, Michel GOSSELIN and Andrd Martf.l corrected the French title

and text.

REFERENCES

AVERINCEV. V.G., 1989. — Sczonnaya dinainika polikhet vysokoarkticheskikh pribrezhnykh ekosistem Zemli Frantsa-Iosifa

(Errantia). [Seasonal dynamics of polychaetes from the high Arctic coastal ecosytcm of Franz-Joseph Land (Errantia).]

Akadcmiya Nauk SSSR Apatity : 1-78. (in Russian).

George. J. D.. & G. IlARTMANN-SCHRODER, 1985. — Polychaetes: British Amphinomida, Spintherida and Eunicida. Synop.

Brit. Fauna (New Series), 32 : 1-221.

HILBIG, B. & J.A. Blake, 1991. — Dorvilleidae (Annelida: Polychaeta) from the U.S. Atlantic slope and rise. Description of

two new genera and 14 new species, with a generic revision of Ophryotrocha. Tool. Seri.. 20 (2) : 147-184.

Lewis. C.F.M.. & S.M. Blasco, 1990. — Character and distribution of sea-ice and iceberg scours : keynote address. / n :

J.I. Clark (ed). Workshop on ice scouring and the design of offshore pipelines , Calgary. Alberta, April 18-19, 1990.

Canada Oil and Gas Lands AdminisUation. Energy, Mines, and Resources Canada : 57-101.

Oug, E.. 1978. — New and lesser known Dorvilleidae (Annelida: Polychaeta) from Scandanavian and northeast American

waters. Sarsia . 63 : 285-303.

Source

20

Two new species of Branchiomma (Sabellidae) with

redescriptions of closely related species and comments

on Pseudobranchiomma and Scibellastarte

Phyllis KNIGHT-JONES

School of Biological Sciences

University of Wales

Swansea U.K.

ABSTRACT

Species of Branchiomma Kolliker (= Dasychone Sars) are reviewed briefly in order to describe two new species. B.

moebii from the Mediterranean and B. spongiarum from the Faroe Islands. Figures of Branchiomma infarction . B.

bahusicnse and B. arcticum (= Sabellastartc arctica) are given for comparison. SHM helps to show (a) specific differences

in uncini and (b) differences between the stylodes of Branchiomma and the "reduced stylodcs" of Pseudobranchiomma

Jones. Pseudobranchiomma should include some species formerly in the genera Branchiomma and Sabellastartc Kroyer.

RESUME

Deux nouvellcs especes de Branchiomma (Sabellidae) avec des redcscriptions des especes

voisines et dcs re marques sur Pseudobranchiomma et Sabellastarte

Les especes de Branchiomma Kolliker (= Dasychone Sars) sont passecs cn revue brievement pour d^crire deux especes

nouvelles. B. moebii de Mediterranee el B. spongiarum des Ties Feroe. Des figures des Branchiomma infarction. B.

bahusicnse et B. arcticum ( = Sabellastarte arctica) sont donnees pour comparison. L'observation au SEM permet de voir

a) les differences spScifiques entre les uncini et b) les differences entre les stylodes de Branchiomma et les "stylodes

reduits" de Pseudobranchiomma Jones. Pseudobranchiomma comprend quelques especes placees autrefois dans les genres

Branchiomma cl Sabellastarte Kroyer.

INTRODUCTION AND METHODS

Collections from the Mediterranean (Knight-Jones el al. , 1991) and the Faroes (Knight-Jones, 1993)

yielded several species of Branchiomma as diagnosed by Johansson (1927) and Fitzhijgh (1989). Most species

were difficult to name, as descriptions ;tre often inadequate and Johansson's review was partial. It was therefore

KNIGHT-JONES, P.. 1994. Two new species of Branchiomma (Sabellidae) with redescription of cloesely related

species and comments on Pseudobranchiomma and Sabellastarte. hr. J.-C. Dauvin, L. LAUBIER & D.J. Reish (Eds).

Actes de la 4eme Conference internationale des Polychetes. Mem. Mus. natn. Hist, nat .. 162 : 191-198 Paris ISBN 2-

85653-214-4.

192

P. KNIGHT- JONES

necessary to study types (or original material) of all known Brancliiomma species. It soon became clear that many

synonyms in the literature were incorrect. Two new species are compared here with those that are morphologically

most similar and B. bahusiense is figured for the first time. Some species arc close to Pseudobranc/iiomma Jones

(1962), so Pseudobranc/iiomma emersoni Jones was also studied and compared with Brancliiomma and

SabeUastane.

Material has not yet been found of species followed here by asterisks, but these were figured in the original

descriptions. All other listed species have been examined and will be compared elsewhere. Original citations of

most species listed here can be found in Hartman, 1959, under Brancliiomma , Dasychone, or Sabella.

Optical microscopy was helped by a Wild drawing attachment. For scanning electron microscopy (Knight-

Jones & Fordy, 1979) alcohol preserved material was washed in distilled water, placed in a weak cleaning

solution (Decon 75) in an ultrasonic bath for 20-30 sec, rinsed in distilled water, dehydrated in an acetone series,

coated in a polaron MK2 sputter coaler, and examined in a JEOL 35 C. Crown radioles were transferred before

coaling to a Polaron MK1 critical point drying unit using CO2 as the intermediate liquid. Fascicles of chaetae

were also studied by SFM but no specific differences in surface detail could be found.

OLD AND NEW SPECIES OF BRANCHIOMMA

Brancliiomma bombyx (Dalyell), B. lucullanum (delle Chiaje), B. violaceum (Schmarda), B. natalense

(Kinberg), B. capense (McIntosh) and B. pseudoviolaceum (Augener) have their dorsal collar margins fused to the

edges of the narrow faecal groove, but the two new species described here are like most Brancliiomma in having

free dorsal margins separated by a wide gap. Their uncinal crests have many rows of teeth, as in Brancliiomma

infarct urn (Kr0yer = Dasychone decora Sars), B. inconspicuum (Sars), B. bahusiense Johansson (as B. infarct a var.

bahusiensis ) and B. arcticum (Ditlevsen = Sabellastarte arctica Ditlevsen) with which they are compared.

The radioles of the new species lack the ‘macrostylodes’ (defined as being three or more times the length of

neighbouring pairs, see KNIGHT-JONES et al., 1991), which are seen in distal halves of dorsal mid lateral radioles

in B. nigromaculatum (Baird) (= Sabella crispa Kr0yer, = Dasychone ponce Treadwell), B. boholense (Grube),

B. bairdi (McIntosh), B.japonicum (McIntosh), B. conspersum (Fillers) (= ? Dasychonopsis arenosa Treadwell),

B. maculatum (Fischli)*, B. gravelyi (Aziz)*, B. loandense (Treadwell) and B. pererai de Silva (as B.cingulata

var. pererai) [some of the latter four species may be synonyms of the others]. Some species which lack distal

macrostylodes, e.g. B. Iiavaiicum (Kinberg), B. cingulatum (Grube), B. luctuosum (Grube), B. curtttm (Fillers),

B. corolliferum (Fillers) and B. galei (Augener), differ from the two new ones in having thoracic uncinal crests

with just two or three rows of few teeth (e.g. Fig. 4g-h). At least the last five of these are distinct species and

will be described elsewhere.

Brancliiomma moebii sp. now — Holotype ZMHUB 2304a (Fig. la-d, f-k); paratype ZMHUB 2304b (Fig.

le) Rovinj, N Adriatic.

Dasychone lucullana — Saint-Joseph, 1906 : 241. Cannes (MNHNP A3 11). Brancliiomma species A. —

KNIGHT-JONES et al ., 1991 : 847. One specimen found in gulley 3-13 m deep SW of Harem point, Bodrum,

Turkey (personal collection).

Additional material: a single specimen from the Bay of Muggia, Trieste (ZMUC), labelled D. lucullana by

Marenzeller.

The following description is based on the holotype, data in parentheses refer to the paratype.

Body 19 by 3.5 (17 by 3) mm with 40 (50) segments of which 8 are thoracic; crown a further 19 (14) mm

long, ventrally involuted at base; radioles 16 (18) on each side connected by a shallow web: each with about 25

(18) pairs of tongue shaped stylodes, larger pairs towards bases of dorsal mid lateral radioles (Fig. lc-d); radiolar

eyes almost obscured by narrow dense pigment bands lying just anterior to bases of (usually) alternate pairs of

stylodes (Fig. Id), but eyes not apparent in paler, more distal bands or areas between bands (more eyes occur in

Bodrum material -see below); apinnulate lips of radioles fine, 1 or (less commonly) 2 mm long; dorsal lips

tapered, grooved (with midrib support), about a quarter of length of crown and with fairly narrow lamellae, the

dorsal lamella attached to base of adjacent radiole, without pinnular support; collar with dorsal gap, small ventral

lappets and no veniro-lateral notches; 1st segment (excluding collar margin) about same length as others in thorax

Source : MNHN. Paris

NEW SPECIES OF BRANCHIOMMA (SABELLIDAE) AND COMMENTS ON RELATED GENERA

193

(measured at sides); thoracic fascicles (segments 2 to 8) with about 10 superior chaetae which are slender and

scarcely geniculate, the 'knee' region scarcely wider than shaft (Fig. lg), and about 20 inferior geniculate chaetae

with knee up to twice width of shaft (Fig. 1 h); thoracic uncini with an extensive crest of small compact teeth

(Fig. 4a- b) not usually seen in light microscopy (Fig. If); thoracic tori long (segment 7 with about 30 uncini),

all but die first two tori reaching ventral shields; most fascicles of abdominal chaetae forming compact tufts,

outer chaetae geniculate (Fig. Ik) with Uiick emergent shafts arranged in a C-shape (see Fig. la, insert) around a

cluster of capillary chaetae (Fig. lj); pigment patterns dark brown, most thoracic ventral shields with two IT-

shaped patches, 1st shield widi paired transversely elongate triangles, dorsal side of thoracic parapodia and inter-

ramal area (between fascicles and tori) widi unusually large patches, and dorsal side of abdominal parapodia with

dark triangles.

Fig. 1. — Branehiomma moebii sp. nov .: a, lateral view of holotypc. — b, ventral thorax. — c, dorsal thorax. - d.

whole radiole. — e, ventral view of paratype. — f, thoracic uncinus. — g, superior thoracic chaeta from 7th thoracic

fascicle. h, same, but inferior thoracic chaeta. j. superior capillary chaeta from 6th abdominal fascicle. k.

same, but inferior chaeta. Scales in mm: b as c; g. h. j as k.

This species is named after Professor K. A. MOBIUS (1825-1908) who collected die largest and best preserved

specimens. Me, Clapar£de & Marenzeller labelled their material Dasychone lucullana , but die dorsal lips of

that species are short (lengdis only two times breadth, Knight-Jones et ai , 1991) and die dorsal collar margins

are fused to die sides of the faecal groove.

On the Bodrum specimen some slylodes next to the web are unpaired, die more basal stylodes from dorsal and

lateral radioles are less crowded (more like those of paratype) and eyes are present between most successive pairs

of stylodes. Eyes not associated with colour bands, however, are smaller with fewer ocular units. Eyes are absent

near the base of the crowm (as in Rovinj material) and between a few other random pairs of stylodes. Frequency of

radiolar eyes was not noted in die material from Cannes and Trieste.

The following four species are die only ones widiin Branehiomma which resemble B. moebii in having

widely separated dorsal collar margins and uncinal crests widi numerous small teeth:

- Branehiomma infaremm (Krdyer, holotype ‘Greenland?’, ZMIIC, Fig. 2a-d, j-k) has stylodes like those of B.

moebii (cf. Figs Id; 2e), but larger specimens of B. infaremm (e.g. Malmgren. 1866, NRS 1252, Fig. 2f-g)

have broader, almost subcircular stylodes towards the bases of the dorsal and lateral radioles. Like B. moebii, B .

infarction is plump (body length 4 to 5 dines breaddi, diorax about as long as broad, widi crown up to three

quarters of body lengdi), but B. infaremm differs in having 1) a more extensive collar (especially vcntrally) with

ventro-lateral notches, 2) very numerous chaetae (about 80 in both thoracic and abdominal fascicles), 3) posterior

194

P. KNIGHT- JONES

inferior thoracic chaetae more slender (‘knee* scarcely wider than shaft Fig. 2k), 4) thoracic uncini with a longer

neck (cf. Figs 2h, j: in, 5) no radiolar eyes and 6) no pigment pattern other than bands on crown and indistinct

inter-ramal spots. Many records of infarctum (c.g. Levinsen, 1886; Ditlevsen. 1937: BERTELSEN, 1937;

ZMUC) are in fact the more elongate species Branchiomma arcticum.

- Branchiomma arcticum (Ditlevsen = Sabellastarte arctica Ditlevsen, hololypc, Baffin Bay “Godfhaab Expd".

Stn 86 ZMUC) has similar stylodes to B. moebii (these had been overlooked by Ditlevsen, as most of his

description referred to specimens from station 166, that had suffered histolysis, ZMUC) but differs Irom

B. moebii in having 1) an elongate shape (crown normally 0.25 to 0.4 of body length), 2) first segment about

twice the length of the following one (measured at sides), 3) prominent ventral collar lappets (Fig. 2t & w,

specimens preserved out of and in tubes respectively), 4) tori with gaps between their ventral ends and ventral

shields, and 5) uncini with broader crests of more distinct teeth (Fig. 4e).

- Branchiomma bahusiense Johansson (syntypes from W Sweden, ZMUU 346 a-b; other material from SE

Faroes, NHMT, KNIGHT-JONES 1992) is like Branchiomma moebii in having a plump body and a crown usually

more than half body length (Fig. 2q), but differs in having 1) no radiolar eyes, 2) narrower stylodes; 3) collar with

prominent ventral lappets; 4) short tori not reaching ventral shields (Fig. 2p); 5) broader thoracic uncini with

fewer crest teeth (Fig. 4D and a longer neck (cf Figs If: 2s); 6) more quadrangular, less distinct pigment blotches

on the ventral shields (Fig. 2p), and 7) much smaller inter-ramal spots.

- Branchiomma inconspicuum (M. Sars, in G. O. Sars, as Dasychone ZMUO) has uncini which seem to be

like those of B. moebii but, unlike moebii , has prominent ventral collar lappets and no colouration except liny

inter-ramal spots.

Branchiomma spongiarum sp. now — Holotype ZMUC, Fig. 3, paralype NMMT, both from Sin 377

(BIOFAR Survey) lat. 61043'53" N, long. 05o42'77" W. depth 274 m. - SEof Faroes.

Branchiomma sp. — KNIGHT-JONES, 1992, Faroes shelf (NHMT).

Additional BIOFAR records : Stn. 27, 61°54T0 N, 05o03*80 W, 225 m (1 specimen); Stn 283, 61°07'30 N,

05°51'20 W, 284 m (2); Sin. 375, 6ri0’04 N. 05°43'35 W 245 m (1); Stn 376, 61°09’51 N, 05°45’45 W, 250 m

(1); Stn 378, 61°44'20 N, 05°42’35 W, 258 m (1) and to the north of the Faroes, Stn 352, 62°43T0 N, 07°22’40

W, 354 m (2).

Found in association with sponges, Thenea levis at Stn 377, and T. valdiviae at Stns 375, 376 and 378, hence

the specific name. Sponge spicules were also with the specimen from Stn 27. The holotype is the largest

complete specimen.

Very small species, body 7.5 by 0.8 mm with 34 segments of which 7 or 8 are thoracic; crown a further

5 mm, involuted ventraliy at the base; 12 radioles on each side, each with small tapered tips, about six pairs of

fine stylodes and no eyes; dorsal lips with tapered and grooved midribs, but no pinnular support, blunt tipped, and

about one fifth length of crown; collar with wide gap dorsally and prominent paired ventral lappets; first segment

similar in length to others in thorax; thoracic fascicles small, each with about 12 chaetae, these and those of

abdomen like those of B. moebii (cf Figs lg to k: 3g to j); thoracic uncinal crests more than half the length of

the head, comprising about 20 fairly long and conspicuous teeth (Fig. 4 c, d); thoracic tori short (15 to 22 uncini

in 5th and 6th tori) not reaching indistinct ventral shields (Fig. 3c); inter-ramal spots fairly large and very distinct,

no other colouration.

As this species is found off Faroes, where the morphologically most similar B. bahusiense is also found, the

possibility of it being a juvenile of the latter was considered. In B. spongiarum , however, the stylodes are

relatively longer, compared with both breadth of slylode and width of radiole. Branchiomma bahusiense also

differs in having 1) at least 5 times as many stylodes per radiole, 2) a crown base only 1/16 of crown length,

compared with 1/6 in B. spongiarum , 3) thoracic uncini with a longer neck (cf. Figs 2s; 30, and 4) uncinal crests

smoother in profile (the small teeth lying closer to main fang) covering only half length of uncinal head (Fig. 40.

The blackish-red inter-ramal spots of B. spongiarum are very obvious against the pale body, whereas the minute

inter-ramal spots of B. bahusiense are less noticeable against a background of pale pinkish-fawn. None of 19

Faroes specimens of B. bahusiense occurred at stations where B. spongiarum was found (although depths, 235-

732 m. were similar) nor does B. bahusiense occur in association with sponges. It was commonly with Sertella.

Source :

NEW SPECIES OF BRANCHIOMMA (SABELLIDAE) AND COMMENTS ON RELATED GENERA

195

Brancliiomma infarction, B. arcticum and B. moebii differ from B. spongiarum in having larger bodies, wider

more numerous stylodes, larger uncinal crests of relatively smaller teeth, and longer tori either approaching or

17IG. 2. Brancliiomma inf a return (Kr0ycr. a to d. j, k. m = hololype; f, g. h = Malmgren's, 1866. material): — a. whole

animal lateral view. b, detail of a. — c, ventral thorax. — d. dorsal thorax. — e. whole radiole and enlarged

stylode (Kroyer's MS). — f. dorsal collar and base of crown. - g. dorsal basal stylodes from f. h and j. thoracic

uncini. k. inferior thoracic chaeta. m. ventral view of type before damage (Kr0yer's MS). B. bahusiense

Johansson. Faroes material: n, dorsal thorax. p. ventral thorax. q, whole animal, inserts showing most of a

dorsal radiole. r, inferior thoracic chaeta. - s. thoracic uncinus. B. arcticum (Ditlevsen), Greenland material: t.

ventral thorax. u. dorsal thorax. v. whole animal. — w. lateral thorax (another specimen). — x. dorsal radiole.

— y, thoracic uncinus. z. inferior thoracic chaeta. Scales in mm: c. d. as b; j. s and y as h: n as p; w and u as t:

z as k.

196

P. KNIGHT- JONES

touching the ventral shields. Branchiomma moebii further differs in having shorter ventral collar lappets, very

large inter-ramal spots, and a distinctive colour pattern. Branchiomma inconspicuum differs in having more

numerous teeth on the uncinal crests.

dorsal thorax. c, dorsal radiole. f, thoracic uncinus. — g and h, inferior thoracic chaetae, side and face view

respectively. j, superior thoracic chaeta. Scales in mm: c and d as b; g and j as h.

STUDIES ON PSEUDOBRANCHIOMMA JONES AND SABELLASTARTE KR0YER

JONES (1962) suggested the genus Pseudobranchiomma for P. emersoni , a species like Branchiomma but with

four thoracic segments and radioles with reduced sty lodes and without eyes. FlTZHUGH (1989) suggested three

more characters separating Pseudobranchiomma from Branchiomma : radioles bearing flanges; dorsal lips without

pinnular support; and abdominal fascicles with longer chaetae in the middle of the group. However, the latter

character is also found in Branchiomma ; presence or absence of pinnular support for a dorsal lip is rarely

important (the holotype of P. emersoni, AMNH, has one of its lips free and the other attached to a pinnule);

whilst possession of few thoracic segments is no more than a specific character, examples occurring in

Branchiomma (e.g. B. curta) and other genera (e.g. Perkinsiana Knight-Jones, 1983). Pseudobranchiomma may

thus seem closer to Branchiomma than envisaged by Jones (1962) and FlTZHUGH (1989).

Source :

NEW SPECIES OF BRANCHIOMMA (SABELLIDAE) AND COMMENTS ON RELATED GENERA

197

FIG. 4. — SEM of thoracic uncini (a to h) and radioles (j tom). — a and b, Branchiomma moebii sp. now — c and d, B.

spongiarum sp. nov. e, B. arcticum Dillcvsen. — f, B. bahusiense Johansson. — g, B. cingulatum (Grube). — h.

B. curt um (Ehlers). j, Pseudobranchiomma emersoni Jones from Cape Verde Islands (NHML). — k. P. orientalis

(McIntosh) from Hong Kong (NMWC). m. Branchiomma moebii sp. nov.

The so-called reduced stylodes of Pseudobranchiomma, however, are very different from Branchiomma

stylodes, which are epithelial flaps arising more or less tranversely to the axis of the radiole (Fig. 4m).

Pseudobranchiomma 'stylodes' are mere discontinuities in paired flanges along the radioles (Fig. 4 j,k). Similar

notched flanges are seen in Sabella (Dasyclione) serratibranchis Grube, Sabella tricolor Grube, Dasychone picta,

D. orientalis McIntosh, D. kumari* Aziz, 1). odhneri Fauvel and Sabella zebuensis McIntosh. These species

should be included in Pseudobranchiomma, although some seem to be synonyms of others (study in progress).

The notches in odhneri and zebuensis, however, are sparse and vestigial. Both species have been placed in

Sabellastarte by Day (1951) and Hartman (1959). Day (1951) synonymised odhneri with Sabellastarte tonga

(Kinberg), but present studies show the two species to be distinct, yet similar enough to place S. longa in

Pseudobranchiomma loo, amending die only significant generic character to:- radioles with paired, longitudinal

flanges, usually notched, but notches sometimes vestigial or absent. Pseudobranchiomma odhneri and P. longa

both have eyes on the radioles so that character too should be amended to :- radioles with or without eyes. They,

like the other species here placed in Pseudobranchiomma, have their dorsal collar margins free, not fused to the

sides of the faecal groove.

1 here seems to be no type material of Sabellastarte indica (Savigny) (type species designated by Hartman,

1959), but species agreeing with Savigny's definition (under "Tribu Sabellae Astarte”) have a double row of

[interdigitating] radioles, as in Sabellastarte magnifica (Shaw) and other species under study. These lack radiolar

flanges (and eyes) and have dorsal collar margins fused to the midline groove. The latter character is not

necessarily generic, for it varies within Branchiomma and both states (fused and free) can occur in a single species

(Megalomma heterops Perkins, 1984). Studies on Pseudobranchiomma and Sabellastarte are continuing so

characters other than radiolar flanges may be found to separate these genera more conclusively. Like Sabellastarte,

Branchiomma lacks such flanges.

Source :

198

P. KNIGHT- JONES

ACKNOWI JUDGMENTS

I am much indebted for facilities, material and information to the directors and staffs of the following

museums (shown in text above by initial letters): The American Museum of Natural History, New York

(AMNH): the Natural History Museums of London (NHML), Paris (MNHNP), Stockholm (NRS) and Thorshavn

(NHMT); the National Museum of Wales, Cardiff (NMWC) and the Zoological Museums of the Humboldt

University, Berlin (ZMIIUB) and of the Universities of Copenhagen (ZMUC), Oslo (ZMIJO) and Uppsala

(ZMUU). I am also very grateful to the Institute for Water Products Research, Bodrum, and die School of

Biological Sciences, Swansea, for research facilities, and to Drs M.R. FORDY for help with SEM, Arne

N0rrevang and Anne Klitgaard for material of Branchiomma spongicinim and information on associated sponges,

Zeki Ergen for help in collecting B . moebii , Mary E. PETERSEN for information about Kroyer's manuscript.

Thomas IE Perkins for valuable comments on this manuscript, die Systematics Association for a Wild

microscope with drawing attachment, die Ray Society and Royal Society for travel grants and the Linnean

Society of London (Applcyard Fund) for SEM costs.

REFERENCES

BERTELSEN, E.. 1937. Contributions to the animal ecology of the fjords of Angmagssalik and Kangerdlugssuaq in East

Greenland. Mcddr Gronland. 108 : 1-58.

Day, 1951. The polychaete fauna of South Africa. Part 1. The intertidal and estuarine Polychaeta of Natal and

Mozambique. Annls Natal Mus .. 12 : 1-67.

DlTLEVSEN. IE. 1937. Polychaeta. The Godthaab Expedition 1928. Meddr Gronland, 80 : 1-64.

FlTZHUGH, K.. 1989. A systematic revision of the Sabcllidae - Caobangiidae - Sabellongidac complex (Annelida :

Polychaeta). Bull. Amer. Mus. nat. Hist. 192: 1-104.

HARTMAN. O.. 1959. Catalogue of the polychaetous annelids of the world. Occ. Bap. Allan Hancock Fdn. 23 : 1-628.

Johansson. K.E.. 1927. — Beitriige zur Kenntnis der Polychaeten-Familien Hermellidac. Sabcllidae und Serpulidae.

Zool. Bidr. Upps.. 11 : 1-184.

JONES, M.E.. 1962. — On some polychaetous annelids from Jamaica, the West Indies. Bull. Amer. Mus. Nat. Hist.,

124 : 169-212.

KNIGHT-JONES. P.. 1983. — Contributions to the taxonomy of Sabcllidae (Polychaeta). J. Linn. Soc. (Zool.), 79 : 245-

295.

KNIGHT-JONES. P., 1992. Sabellariidae and Sabcllidae of the Faroes including some forgotten species. In: Marine

Biology and Oceanography of the Faroe Islands (BIOEAR). A. NorrevaNG (ed )Arbok 1991-92. Nordurlandahusid i

Foroyum, Torshavn. 100 pp.

Knight -Jones, P. & FORDY, M. R.. 1979. Setal structure, functions and interrelationships in Spirorbidae (Polychaeta,

Scdentaria). Zool. Set.. 8: 119-138.

Knight-Jones, P.. Knight-Jones, E.W. & Ergen, Z.. 1991. — Sabelliform polychaetes mostly from Turkey's Aegean

coast. J. nat. Hist.. 25 : 837-858.

Eevinsen, G. M.R. .1886. Kara-Havcts Ledorme (Annulata). In : C.F. LUTKEN & J. HAGERUP (eds). Dijmphna-Togtets

Zoologisk-botaniske lldbytte. Kobenhavn : 288-303

Malmgren. A.J.. 1866. — Nordiska Hafs-annulater. Opersigt. svenska Vetensk - Akad. Fork.. 22 : 355-410.

PERKINS, Thomas IE. 1984. Revision of Demonax Kinberg. Hypsicomus Grube and Notaulax Tauber, with a review of

Megalomma Johansson from Florida (Polychaeta: Sabcllidae). Broc. biol. Soc. Wash.. 97 : 285-368.

Saint -JOSEPH. A. de. 1906. — Les annelidcs Polychetes des cotes de France (Ocean et cotes de Provence). Annls Sci. nat.

Baris, ser. 9, 3 : 145-260.

Source : MNHN. Paris

21

Redescription of Hipponoa gaudichaudi Audouin &

Milne-Edwards, 1830 (Polychaeta, Amphinomidae)

Jerry D. KUDENOV

Department of Biological Sciences

University of Alaska Anchorage

3211 Providence Drive

Anchorage, Alaska 99508 U.S.A.

ABSTRACT

l*he genus Hipponoa (Polychaeta, Amphinomidae) is monotypic. Hipponoa gaudichaudi Audouin & Milne-Edwards. 1830.

probably represents a highly specialized species whose affinities to amphinomids has been questioned. As part of an on-going

study of Amphinomida, both the genus Hipponoa and species H. gaudichaudi are redescribcd and emended. Affinities with

other taxa of the order are briefly discussed.

RESUME

Rcdescription d 'Hipponoa gaudichaudi Audouin & Milne-Edwards, 1830 (Polychaeta, Amphinomidae)

Redescription de Hipponoa gaudichaudi Audouin & Milne-Edwards, 1830 (Polychaeta. Amphinomidae). Ee genre

Hipponoa est monotypique. Hipponoa gaudichaudi Audouin & Milne-Edwards, 1830, represente probablemcnt une espece tres

specialisee dont les affinites avec les Amphinomidae sont discutees. Comme partie d'une etude en cours sur les Amphinomida,

le genre Hipponoa et l’espece H. gaudichaudi sont redccrits ct emendes. Les affinites avec les autres taxa de Pordre sont

brievement discutees.

INTRODUCTION

On-going studies on the phylogenetic systematics of the polychaete Order Amphinomida (cf. Kudenov, 1994)

have revealed both historical questions and undescribed features for the amphinomid Hipponoa gaudichaudi

Audouin & Milne-Edwards, 1830. For example, McIntosh (1885) suggested that the setae of this species are not

calcareous. This feature, coupled to die fact that H. gaudichaudi lacks a caruncle, led McIntosh and others to

suspect dial it was improperly assigned to the Amphinomidae. Indeed, the Order Amphinomida is highly diverged

in the Class Polychaeta (Dales, 1962; CLARK, 1969). Removal of Hipponoa from the Amphinomidae may result

in establishing another polychaete family (for which precedents exists, see Carus, 1863; Baird, 1870). This

decision cannot be made lightly. The purpose of diis paper is to redescribe and emend the original of

KUDENOV. J.D.. 1994. Rcdescription of Hipponoa gaudichaudi Audouin & Milne-Edwards, 1830 (Polychaeta.

Amphinomidae) in Polychaetes. In: J.-C. Dauvin, L. Laubier & D.J. RE1SH (Eds). Actes de la 4eme Conference inlernationale

des Polychetes. Mem. Mils. natn. Hist, nat .. 162: 199-207. Paris ISBN 2-85653-214-4.

Source : MNHN. Paris

200

J.D. KUDENOV

Hipponoci gaudichaudi, and to address the question by McIntosh and others about the affinity of this species with

the Amphinomidae.

MATERIALS AND METHODS

Materials of Hipponoa gaudichaadi were obtained both from the Smithsonian Institution (USNM) and the

Allan Hancock Foundation Polychaete collection of the Los Angeles County Museum of Natural History (LACM-

AHF). Tissue sections were made following specifications noted by KUDENOV (1977). Preliminary SHM work was

performed at the USNM on preserved specimens held in the general collection.

Family Amphinomidae Lamarck, 1818

Genus Hipponoa Audouin Sc Milne-Edwards, 1830, emended

Hipponoa Audouin Sc Milne-Edwards, 1830: 156. — Cuvier, 1831: 18; Milne-Edwards, 1838: 464. —

Costa, 1841: 270. — Fauchald, 1977: 102.

Hipponoe Cards, 1863: 28. — Quatrefages, 1865: 409-410. — Treadwell, 1939: 177. — Gardiner,

1975: 103. — Non Treadwell, 1931: 3-4, figs. 10-12.

Hipponoe Audouin & Milne-Edwards, 1834: 1 16. — Hoeven, 1850-1856: 244. — Grube, 1850: 289. —

Schmarda, 1861: 134. —Baird, 1870: 239-240. — Fauvel, 1913: 32; 1923: 132. — Horst, 1886: 170. —

Amoureux, 1972: 51.

Hypponne Audouin Sc Milne-Edwards, 1834: 1 17.

Metamphinome Treadwell. 1940: 1.

Emended Diagnosis. — Body of adult fusiform, dorsoventrally flattened, with up to 105 setigers. Prostomium

with five antennae, two pairs of eyes. Caruncle absent. Nuchal organ present. Mouth ventral. Notopodia on

laterum. Ncuropodia on ventrum. Dorsal cirri numbering one per notopodium. Ventral cirri papilliform. Notosetae

all capillaries. Neurosetae retractile, hooks generally bidentatc; may be unidentate. Branchiae planar, bipinnate.

Anus terminal.

Remarks. — This emended diagnosis differs from those presented previously in that a nuchal organ is present,

branchiae are planar and bipinnate, and the anus is terminal. Neurosetal hooks arc generally bidentatc in specimens

with around 30 or fewer segments, and unidentate in a single specimen with 105 segments.

Hipponoa gaudichaudi Audouin Sc Milne-Edwards, 1 830, emended

Figs 1-2

Hipponoa gaudichaudi Audouin Sc Milne-Edwards, 1830: 156-159, PL III, fig. 4-4a-4b. — AUDOUIN &

Milne-Edwards, 1834: 128-129, PI. II, fig. 10-10 bis. — GuSrin, 1829-1843: 1-14, PI. IV. fig. 3, 3A-3D —

Cuvier, 1831 : 19. — Ibanez, 1973: 124.

Hipponoa gaudichaudi agulhana Day, 1967: 122, fig. 3.1 a-e.

Hipponoa gaudichaudi i Cuvier, 1831: 18. — Milne-Edwards, 1838:464.

Hipponoe gaudichaudi Baird, 1870: 239-240. —McIntosh, 1885: 30-33, PI. I, fig. 5, PI. IV, fig. 3, PI. IIIA,

figs. 13-17. —Horst, 1886: 170-171. — Fauvel, 1913: 32; 1914: 89, PI. I, fig. 2, 12; 1923: 132, Fig. 47 1-p:

1936: 19. — Pettibone, 1963: 57-59, fig 13 a-b. — Fauvel Sc Rullier, 1959: 510. — Amoureux, 1972 : 51.

Hipponoe gaudichaudi Hoeven, 1850-56: 244. —Grube, 1850: 289.

Hipponoe Gaudichaudi Stop-Bowitz, 1948: 15.

Hipponoe Gaudichaudi CUVIER, 1830: 199. -Milne-EDwards, 1836: 31-32, PI VIII, fig 4, 4a,b. — Carus,

1863: 28. — Quatrefages, 1865: 410. — Moore, 1903: 793. — WILLEY, 1910: 180. — Sumner, Osburn &

Cole, 1913: 619. — Augener. 1922: 39. — Okuda, 1950: 49, figs a-b.— Gardiner, 1975 : 103, fig. 5 1-m.

Hipponoe gaudichaudi gigantea Hartmann-Schroder, 1981: 24-25, figs. 1, 2.

Hipponoe multibranchiata Hartman 1951: 29, PL 8, figs. 1-2.

Non Metamphinome multibranchiata Treadwell, 1940: 1-2, figs. 1-3.

Hipponoe cranchii Baird, 1870: 240, PL VI, figs. 7-14.

Non Hipponoe elongata Treadwell, 1931: 3-4, fig. 10-12; 1939: 177-178, Fig. 11.

Source : MNHN. Paris

REDESCRIPTION OF HIPPONQA GAUDICHAUDI

201

FIG. 1. — Hipponoa gaudichaudi Audouin & Milne-Edwards : A. prostomiuin and anterior segments of adult, ventrolateral

view. B, same, anteroventral view. -C, same of juvenile lacking median antenna, dorsal view. — D, same, detail of

nuchal organ, dorsal view. — E, neuropodium, ventral view. — F. sheared capillary notofascicle revealing hollow core

(arrow). Abbreviations: 1A, lateral antenna; mA. median antenna; no, nuchal organ; np, neuropodium; or. notosetal

ornamentation; p, palps; pA, palpal antenna; vc. ventral cirrus; vc 1, padlike ventral cirrus of setiger 1; vc 2. ventral cirrus

of setiger 2. Scales : A = 0.2 mm; B = 0.4 mm; C = 0. 1 mm; D = 20 pm; E = 0.2 mm; F = 10 pm.

Source :

202

J.D. KUDENOV

Material examined. — North Adamic Ocean, Gulf Stream, Surface, R/V Albatross, coll. J.E. BENEDICT, 20

specimens (USNM 16311) ; 3 specimens (USNM 32374). — Bermuda, south shore, 5 Aug 1948, coll. II. Ris,

three specimens (LACM-AMF, n5858 from Hartman ledger).

Caribbean Ocean, Panama, Galeta Point, 14 Jul 1976, in sargassum rafts washed onto reef Bats, coll.

G. HENDLER, 1 specimen (USNM 58724). — Louisiana, Grand Isle, coll. H. Bennett, 4 (LACM-AHF,

n 10183 from Hartman ledger).

North Pacific Ocean, 30°50'N, 121°35'W, 29 May 1954, in Lepas fascicularis Ellis & S dander, coll. D.

HENRY, 19 specimens (USNM 32366); 27°56'N, 1 19°36'W, 23 Apr 1954, in L. anatifera Linnaeus, two specimens

(USNM 32367); 27°56'N, 1 19°36’W, 23 Apr 1954, in L. fascicularis Ellis & Solander, six specimens (USNM

32368); 28°40’N. 129°35’W, Jun 1955, in L. anatifera Linnaeus, two specimens (USNM 32369); 30° N, 1 18° W, 4

May 1954, one specimen (USNM 32370); 26°12'30" N, 1 18027’ W, 24 Aug 1954, in L fascicularis Ellis &

Solander, two specimens (USNM 32371); 30° 50’N, 121°35'W, 29 May 1954, in L. pectinata Spcngle, one

specimen (USNM 32372); 27°56'N, 119°36'W, 23 Apr 1954, in L anatifera Linnaeus, 5 specimens (USNM

32373); Off Japan, 28°02’N, 155°58'E, 29 Apr 1970, coll. G. Chase, 2 specimens (USNM 43205). — ?Pacific

Ocean, 9 Jun 1961, coll. D. Davenport, seven adults + numerous juveniles (LACM-AHF).

Description. — Body of adults fusiform, dorsoventrally flattened, 24-105 mm long, 5-18 mm wide without

setae, totalling 20-46 setigers; dorsum broadly exposed. Color in life bright orange.

Prostomium a small, single, rhomboid-shaped lobe, with 5 cirriform antennae (Fig. lc-d). Median antenna

about as long as prostomium, lacking ceratophore (Fig. 2a). Lateral antennae arising from frontal, dorsomedial

surface, about 0.6 times length of median antenna (Fig. 2a). Palpal antennae arising from anterolateral surfaces of

palps, somewhat more stout and shorter than lateral antennae (Figs la-b; 2b). Eyes numbering two pairs, located

anterior to median antenna, where prostomium is widest, all small, inconspicuous. Caruncle absent. Nuchal organ

present as ciliated patch on posterior prostomium, best observed in specimens with fewer than 15-18 setigers (Figs

lc-d; 2a). Palps fused into single lobe, forming upper lip of mouth and short midventral groove (Figs la-b; 2b).

Mouth ventral, opening between setigers 1-2; setigers 1-2 forming lateral lips of mouth; setiger 2 posterior lip

(Figs la-b; 2b).

Setiger 1 with setigerous notopodia, neurosetae absent, neuropodia only represented by pad-shaped ventral cirri

(Figs la-b; 2b). Parapodia biramous, setigerous from setiger 2 to end of body; rami more widely separated from

one another compared to setiger 1. Notopodia as transverse ellipses in outline in dorsal view, confined to extreme

dorsolaterum; notopodial lobes not raised above general body surface. Neuropodia circular to slight transverse

ellipses in outline in ventral view, confined to ventrum (Fig. le); neuropodial lobes resembling retractable papillae

surrounded by thick, glandular collars of tissue (Fig. le) with papilliform ventral cirri.

Parapodial cirri present on all setigers. Dorsal cirri cirriform, with basal cirrophore two times longer than wide,

distal style about 2-3 times longer than cirrophore; arising from body wall behind inferior notosetal fascicle

margin, not within notosetal fascicle. Ventral cirri papilliform, lacking basal cirrophores, slightly longer than wide;

arising medially from collar of neuropodium that encircles ncurosetal fascicles (Figs la-b, e; 2b).

Notosetal fascicles with numerous setae directed laterally in all setigers. Notosetae hollow (Fig. If, arrow),

slender capillaries with file-like teeth on shafts (Fig. la-b, 0, calcareous, accessory subdistal spurs absent, tapering

distal ly to fine, entire tips (Fig. la-b). Neurosetae from setiger 2 of one kind; chitinous, solid, distally bidentate

hooks with longitudinal striae, numbering around 10 per fascicle (Fig. le). Notoaciculae inconspicuous,

capillariform, numbering 3-5 per fascicle, limited to posterior notopodial margin. Neuroaciculae from setiger 2

distally curved, distally embedded in clear cuticular matrix, non-emergent, numbering 8 per fascicle, in single,

long, dorsal rows along superior or outer lateral margins of neuropodia (Fig. 2c).

Branchiae bipinnate, pinnae branching alternately off primary branchial axis, each pinna in turn branching up

to 6 times basally and having fewer branches distally (Fig. 2d-e); pattern more conspicuous in small specimens.

Branchiae present from setiger 3 to end of body, numbering 1 pair per segment, tending to be planar, particularly

in small specimens (Fig. 2d) than in larger ones (Fig. 2e). Branchial bases broad, arising posterodorsally to dorsal

cirri, not extending beyond notosetae. Branchiae gradually increasing in length and development to midbody,

gradually becoming shorter, less developed to end.

Pygidium with terminal anal cirrus; anus opening through anal cirrus (Fig. 2f).

Distribution. — Cosmopolitan in tropical and warm temperate oceans.

Remarks. — Hipponoa gaudicliaudi has been reported from numerous localities throughout the world, and its

description has not significantly changed since AUDOU1N & Milne-Edwards (1830) first described and Baird

(1870) later emended it. As presently understood, H. gaudicliaudi appears to be a highly modified and specialized

member of the Amphinomidae, probably reflecting the fact dial it is an inquiline of barnacles {Lepas species:

Source :

REDESCRIPTION OP HIPPONOA GAUDICHAUDI

203

Baird. 1870: Aucener, 1910: Kudenov, 1977). Although H. gaudicliaudi retains many features of the

Amphinomida, it is generally quite unlike most amphinomids (Gustafson, 1930 ; Kudenov, 1994).

FlG. 2. Hipponoa gaudichaudi Audouin & Milne-Ed wards: A — B, Proslomium showing only three of five antennae and

setiger 1, dorsal view. - C, neuroaciculae. — D. hipinnate branchia from right setiger 10. anterior view. — E, same, from

left setiger 13, anterior view. — F, pygidium, dorsal view. Abbreviations : see legend for Fig. 1. Scales : 1 = 0.25 mm, F; 2

= 10 pm, D: 3 = 30 pm, E and 5 pm. C: 4 = 0.2 mm. A, B.

For example, H. gaudicliaudi differs from the general amphinomid pattern in that its body is strongly flattened

and fusiform, and is die only known genus with a continuous midventral groove. Its prostomium is strongly

reduced to a single lobe with palpal antennae arising from the anterolateral margins of die prostomium. Palps are

extremely short, narrow, and fused medially, and are confined to the ventral area lying between the moudi and

prostomium (Fig. 2b; Kudenov, 1993). The mouth is present very close to die prostomium at the junction of

setigers 1-2 (Fig. 2b). Setiger 1 is dorsally complete, and is not interrupted by a caruncle. Notopodia arise from die

extreme dorsolaterum; neuropodia from the ventrum. The notosetae are endrely nonspurred capillaries; it is the

only presently known genus of die family in which the notosetae are represented solely by capillaries. The dorsal

cirri arise directly from the body wall as diey do in the Euphrosinidae, and not from within die notopodial field as

is typical of Amphinomidae. Obviously, H. gaudicliaudi is quite unlike the Amphinomidae sensu lato in many of

its features.

Additional traits either confirmed or newly discovered as part of diis study can be added to this list.

H. gaudichaudi is characterized by die: 1) lack of a caruncle: 2) a poorly ciliated, mound-shaped nuchal organ; 3)

absence of bodi neuropodia and ncurosetac in setiger 1: 4) reduced dorsal cirri in seuger 1: 5) lack of cirrTphores

on ventral cirri; 6) hollow calcareous notosetae; 7) solid neurosetae that may be chitinous; 8) planar, bipinnate

branchiae; and 9) a terminal anus opening through an anal cirrus. All except the first and third of these traits are

newly reported.

The nuchal organ is poorly ciliated, and more conspicuous as a mound-shaped lobe on the posterior

prostomium in juveniles and subadults than in larger individuals, such as functionally mature females. This finding

204

J.D. KUDENOV

may be expected, given the fact that H. gaudichaudi is a protandric hermaphrodite (KUDENOV, 1977). It is

hypothesized that immature individuals rely on nuchal organs and chemical senses to a much greater extent

compared to mature worms to maintain body contact with their brooder, to obtain food, and to subsequently locate

other barnacles. The nuchal organ must therefore be relatively better developed in immature individuals.

The lack of neuropodia and neurosetae in setiger 1 was previously noted by Day (1967) who made no further

comments about its significance. In this specialized amphinomid, setiger 1 is strongly modified and forms the

lateral margins of the mouth. It is so small that most light microscopical observations of this segment have lead

workers to assume the presence of neuropodia and neurosetae. The ventral cirri of setiger 1, which are both

reduced and very close to the mouth, may function in feeding. Moreover, H. gaudichaudi is the only described

amphinomid species in which ventral cirri lack cirriphores.

McIntosh (1885) particularly, and other workers generally, questioned whether the setae of H . gaudichaudi

are calcareous as those of other amphinomids. He strongly suggested that H. gaudichaudi is not typical of other

amphinomids whose setae produce gas bubbles when they are treated with weak acetic acid. McIntosh conveys

die impression that he would have assigned Hipponoa to another taxon if he had had additional evidence. Both

Carus (1863) and Baird (1870) had previously proposed die Hipponacea and Hipponoidae, respectively. SEM

studies revealed notosetal ornamentation (Fig. 10 usually associated with the calcareous setae of the

Amphinomida (Kudenov, 1993, 1994). Tissue sections through notosetal fascicles tend to splinter die setae of

non-decalcified specimens, leaving fragments of a clear outer layer assumed to be calcareous (Kudenov,

unpublished). H. gaudichaudi is clearly related to die Amphinomidae also by die fact diat its notosetae are hollow

(Fig. If), a feature shared by all other members of die order (Kudenov, 1994). However, its neurosetal hooks may

not be calcareous. All appear solid in bodi SEM and tissue section preparations, lack ornamentation referred to

above, and have densely packed longitudinal striae reminiscent of chitinous setae. Confirmation of these

observations awaits the receipt of fresh specimens. These setal data are presently insufficient to define

relationships between Hipponoa and other Amphinomida; they will eventually be refined and included in a

cladistic evaluation of the order Amphinomida (KUDENOV. 1994).

The branchiae of H. gaudichaudi have generally been described as being tuft-like, arborescent or dendritically

branched and bushy. All such terms are misleading. In fact, die branchiae are all bipinnate and planar (Fig. 2d-e), a

condition most obvious in juveniles which is clearly retained in adults, and reminiscent of those found in the

Chloeia species complex. However, primary branchial axes in Hipponoa gaudichaudi may be contractile; degrees

of contraction ranging from a long, slender zig-zagging to a stout, basal axis sometimes obscuring die bipinnate

pattern. Bodi taxa also have lateral cirri (mistaken for true dorsal cirri which are present in setigers 1-4 of Chloeia)

arising directly from the body wall and outside the notopodial field. No attempt to imply common ancestry

between these taxa is intended.

Another overlooked character in H. gaudichaudi is die presence of a terminal anus diat opens through die anal

cirrus (the presence of a dorsal anus has been assumed [e.g., Fauvel, 1923]). In other members of die

Amphinomidae, die anus opens on the dorsum of the last few body segments, above an associated, unpaired anal

papilla. The anus of Euphrosinidae is terminal, and opens between or above paired anal cirri (Kudenov, 1994).

The unusual anus of H. gaudichaudi presumably reflects its highly specialized life style, enabling it to void its

feces widiout fouling either itself or its host. This point can only be answered by studying live specimens of both

the worm ai id its host.

The synonymies listed above are not intended to be exhaustive. Analysis of the earliest literature shows

AUDOUIN & Milne-Edwards (1830) original record from Port Jackson, Australia, was quoted by subsequent

workers. Baird (1870) published what appears to be the second record of the species from die eastern equatorial

Atlantic and Madeira. He described a second species, H. cranchii , which his illustrations show to be a juvenile

Amphinome ( Irostrata ), and not a second species of Hipponoa. The diird record of H. gaudichaudi was from die

Challenger expedition, and MclNTOSH (1885) provided extensive observations about it, including die presence of

capillary notosetae having distal ly forked ends. Such notosetae have not been reported for H. gaudichaudi at any

other lime prior or subsequent to his work. Horst (1886) represents die fourth record, after which time the species

was more commonly encountered. Day (1967, Fig. 3.1.a-e) later described the subspecies, H. gaudichaudi

agulhana , based on the absence of notosetae as described by McIntosh (1885). It is suggested that McIntosh

observed frayed or damaged notosetae that appeared distally forked. Another, H. gaudichaudi gigantea Hartmann-

Schroder (1981) was distinguished on the basis of body size and hook morphology. Although the specimens she

examined were up to 105 mm long, neurosetal hook morphology may reflect size-dependent relationships instead

of polyploidy, as implied by Hartmann-SchrOder. Moreover, distinction between the terms "Normalform" and

Source :

REDESCRIPTION OE H1PPONOA GAUDICHAUDI

205

Riesenform used by I Iartmann-SchrGder to describe H. gaudichaudi gigantea are typological, and seem to

preclude a continuum or morphological change associated with allometric growth.

The genus Hipponoa supposedly represents three described species (Fauchald, 1977) including

H. gaudichaudi, H. cranchii Baird, 1870, and H. elongata Treadwell, 1931. Metamphinome mullibrancliiata

Treadwell, 1940 was referred to Hipponoa by Hartman (1951) and H. gaudichaudi by Pettibone (1963). All

previous descriptions and illustrations are sufficiently clear to indicate H. cranchii is probably a juvenile

Amphinome, and H. elongata is most certainly a Linopherus- like species. Therefore, die genus Hipponoa is

presently monotypic.

In summary, the species description of Hipponoa gaudichaudi is emended with certain observations confirmed

and additional characters newly reported. The species seems to be highly specialized and derived: departs

substantially from the general features normally attributed to die Amphinomidae (KUDENOV. 1994); and seems to

be cosmopolitan in tropical, subtropical and warm-temperate oceans. But is this taxon truly cosmopolitiui and

monotypic? Only a thorough systemauc study involving specimens from various points throughout its range can

answer these and odier questions.

ACKNOWI JEDGEMENTS

I am indebted to Kristian FAUCHALD, Greg Rouse and Linda Ward, all from the National Museum of Natural

History, and Len HlRSCH, Office of International Relations, Smithsonian Institution, Washington D.C., for dicir

assistance, support, encouragement and insights offered throughout this study. I especially thank Greg ROUSE for

his assistance widi die SEM. I also diank Kirk FlTZHUGH and Leslie Harris, Los Angeles County Museum of

Natural History, for loan of materials and for verifying literature citations. Editorial comments made by Kirk

FlTZHUGH and an anonymous reviewer improved this paper. Debra LACH1NSK1 provided the initial version of die

abstract in French.

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Source ; MNHN, Paris

22

Sabellariidae (Annelida, Polychaeta)

from south America

Paulo da Cunha LANA* and Claudia Silvia BREMEC **

* Centro de Estudos do Mar, Universidade Federal do Parana

Av. Beira-Mar. s/n, 83255-000 Pontai do Sul, Parana, Brazil

** Instituto Nacional de Investigacion y Desarrollo Pesquero

C. C. 175. 7600 Mar del Plata, Argentina

ABSTRACT

This paper summarizes the present taxonomic knowledge of Sabellariidae Johnston. 1865 from South America. Records of

ldanthyrsus annatus Kinberg, 1867, /. pennatus (Peters, 1854). Phragmatopoma attenuate Hartman, 1944, P. peruensis

Hartman, 1944. P. virgini Kinberg, 1867. P. moerchi Kinberg, 1867, P. lapidosa Kinberg. 1867, Sabellaria bella Grube. 1870,

S. bellis Hansen, 1882. S. fissidens Grube, 1870, S. minuta Carrasco & Bustos. 1981. S. nanella Chamberlin, 1919, and

S. wilsoni Lana & Gruel. 1989 are included. Regional synonymies, diagnoses, taxonomic remarks, and occurrence information

are provided for each species, together with an identification key and distributional maps. Discontinuous distribution patterns

of the continental sabellariid fauna may be only partially attributed to incomplete sampling. Many species seem to have

restricted distribution ranges. It is hypothesized that the dispersion patterns of sabellariids in South America do not conform to

the dispersal paradigm that could be expected from then active larval phases.

RESUME

Sabellariidae (Annelida, Polychaeta) d'Amerique du Sud

Petal actuel des connaissances sur les Sabellariidae Johnston. 1865 d'Amerique du Sud est presente. Les lieux de recoltcs

de ldanthyrsus annatus Kinberg, 1867. I. pennatus (Peters. 1854). Phragmatopoma attenuata Hartman. 1944. P. peruensis

Hartman, 1944. P. virgini Kinberg, 1867, P. moerchi Kinberg, 1867. P. lapidosa Kinberg. 1867, Sabellaria bella Grube. 1870.

S. bellis Hansen, 1882. S. fissidens Grube. 1870. S. minuta Carrasco & Bustos, 1981, S. nanella Chamberlin, 1919 et S. wilsoni

Lana & Gruel, 1989 sont donnes. Les synonymies pour cette region, des diagnoses, des remarques taxonomiques et des

informations sur les recoltes de chaque espece soul fournies. Une cle d'identification des especes et des cartes de distributions

soul egalemenl donnees. La distribution discontinue observee 1c long des cotes d'Amerique du Sud pourrait etre due a fabsence

d’observations dans certaines regions. Cependanl. beaucoup d’especes semblent avoir une distribution reduite. I/hypothcse

selon laquellc le mode de dispersion des Sabellariidae d’Amerique du Sud n'est pas conforme au modele correspondant a une

vie larvairc active est avancee.

INTRODUCTION

The Sabellariidae Johnston, 1865 currently comprises seven genera and about 65 species of colonial or non¬

colonial tube-building worms. Some species construct reefs of great extent in temperate or tropical regions.

Lana P., &C. S. BREMEC. 1994. Sabellariidae (Annelida: Polychaeta) from south America. In\ J.-C. Dauvin,

L. LAUBIER & D.J. REISH (Eds), Actes de la 4cme Conference intemationale des Polychetes. Mem. Mus. natn. Hist. not.. 162 :

211-222 Paris ISBN 2-85653-214-4.

Source : MNHN. Paris

210

P. I, AN A & C. S. BREMEC

Representatives of this family occur from nearshore to oceanic depllis (UEBELACKER, 1984).

The present recognized genera are Phalacostremma Marenzeller, 1895, Monarch os Treadwell, 1926,

Gunnarea Johansson, 1927. Lygdamis Kinberg, 1867, Idanthyrsus Kinberg, 1867, Phragmatopoma Moerch, 1863,

and Sabellaria Savigny, 1818, widi only the three latter previously reported from South America. The regional

sabellariid fauna was hitherto poorly known. Relevant taxonomic literature is widely scattered and die level of

consistency in identifications appears to be rather low.

In this paper, we summarize the present taxonomic knowledge of Sabellariidae in South America. We have

attempted to include all published records from this area. Synonymies, diagnoses and the known geographic range

are provided for each species, together with an identification key and distributional maps.

This work is partially based on literature information, and we have not attempted to resolve disputed

taxonomic problems. Some taxonomic assignments are tentative, but can serve as background information for

future revisions based upon type-specimens or topotypes. Specific names are cited as listed in the original

references.

SYSTEMATIC^

Idanthyrsus Kinberg, 1867

Type-species: Idanthyrsus armatus Kinberg, 1867

Idanthyrsus armatus Kinberg, 1867

Idanthyrsus armatus Kinberg, 1867: 349. — JOHANSSON, 1927: 90. — MONRO, 1930: 177, fig. 73. — MONRO,

1933: 1066, fig. 14. — Monro. 1936: 172. — Hartman, 1944: 336, pi. 31, fig. 36. — Hartman, 1953: 10. —

Hartman. 1966: 73, pi. 24. figs 2-6. — Hartman, 1967: 150. — RlNGUELET, 1969: 212. — FAUCHALD 1972'

530. pi. 55, figs h-j. — Orensanz, 1974: 55. — FAUCHALD, 1977: 54. — RULLIER & AMOUREUX, 1979: 188. —

Carrasco & Bustos, 1981: 170, figs 8-1 1. — Hartmann -Schroder, 1983: 271. — Laverde-C, 1986- 128

Pallasia sexungula — Fillers, 1897: 125, pi. 8, figs 194-202. — Ehlers, 1900: 220. — Ehlers, 1901a: 267

Pallasia armata — Ehlers, 1901b: 195.

Sabellaria macropalea — Prait, 1901 : 1 3, pro parte

Pallasia pennata — Fauvel, 1941: 291.

Diagnosis — External paleae directed outward and plumelike, serrated, with a nearly straight shaft; spinelets

widely separated and curved outward (Fig. la). Inner paleae smooth hooks with narrow transverse striae. Uncini

with a double lateral row of 8 teeth, in addition to one median tooth at superior end. 2-4 pairs of nuchal hooks.

Maximum reported length 59 mm.

Distribution — South America: Pacific coast of Colombia; Valparaiso, Concepcion, and other sites of

Genual Chile: Magellan Strait: Beagle Channel; Cape Horn: Malvinas-Falkland Islands; South Georgia Island;

continental shelf off Patagonia and northern Argentina. Odier records: Western Mexico; British Columbia; Alaska;

Australia; Japan.

Remarks — /. armatus has been usually reported from cold waters in die southern and northern sectors of the

Pacific and in the southern West Atlantic. The range of the closely related I. pennants (Peters, 1854) appears to be

circumtropical, extending northward or southward from that of I. armatus. The zones of overlapping are few and

have been reported by Monro (1933), Rioja (1962), FAUCHALD (1977), and Laverde-Castillo (1986) for die

Pacific coasts ol Mexico, Panama and Colombia. However, records of I. armatus from Panama are doubtful, since

Gorgona Island, cited in the literature as a Panamian locality (Monro, 1933; Fauchai.d, 1977) is in fact off the

Colombian coast, about 600 km south of die Canal Zone. In addition, Monro’s illustration of an external opercular

palea (1933, p. 1065) clearly differs from those later provided by Hartman (1944) or Day (1967).

Neither I. armatus nor /. pennants have been recorded from the extensive tropical and subtropical Brazilian

coast. Ihe northern range of /. armatus along the Western Atlantic is clearly conditioned by the Subtropical

Convergence, north of La Plata River, where the colder waters of die Malvinas-Falklands Current meet the more

saline and warmer waters of the Brazil Current.

I. at matus and /. pennatus are known to ditler only in minor details of die outer paleae dentation, tapering in

die first and slender in the second. Besides that, shafts of the outer paleae are curved in /. pennatus and straighter

in /. at matus. femperature dependent variation in the morphology of polychaete hard parts has been previously

Source : MNHN, Paris

SABELLARIIDAE FROM SOUTH AMERICA

211

described by REISH (1977). A careful analysis of this problem should be undertaken in order to clarify the

taxonomic relationships of those species.

Idanthyrsus pennatus (Peters, 1854)

Sabellaria (Pallasia) pennata Peters, 1854: 613.

Idanthyrsus regalis — Chamberlin, 1919: 487, pi. 74, figs 1-8.

Idanthyrsus pennatus — JOHANSSON, 1927: 88. — MONRO, 1930: 176. — MONRO, 1933: 1065, fig. 13. —

Hartman, 1939: 19. — Fauciiald & Reimer, 1975: 90. — Fauchald, 1977: 54. — Laverde-Castillo, 1986:

128.

Diagnosis (modified from Day, 1967) — Opercular crown with two rows of long paleae. External paleac with

curved shafts and slender denticles (Fig. lb). Inner paleae smooth with tapering tips. 1-2 pairs of stout nuchal

hooks.

Distribution — South America: Pacific coast of Colombia and Ecuador; Galapagos Islands. Other records:

Western Panama and Mexico; Mossambique; South Africa; Tropical Indo-West Pacific from Madagascar to Japan.

Remarks — Taxonomic affinities and distribution range of /. pennatus and /. armatus were discussed above.

Phragmatopoma Mocrch, 1863

Type-species: Phragmatopoma caudata Moerch, 1863

Phragmatopoma attenuata Hartman, 1944

Phragmatopoma attenuata Hartman, 1944: 352, pi. 38, figs 90-96, pi. 39, figs 100-101. — Fauchald, 1977:

54. — Laverde-Castillo, 1986: 128.

Sabellaria ( Phragmatopoma ) virgini — MONRO, 1933: 1062, fig. 1 1.

Diagnosis (modified from Hartman, 1944) — Opercular crown slender, prolonged and asymetrical in lateral

view. External opercular paleae with a unique distal appendage, consisting of a palmately filamentous membrane,

directed nearly at right angles to the main shaft. Shaft with a recurved tooth on the ventral-facing side and weakly

scabrous on the upper surface (Fig. lc).

Distribution — South America: Ecuador, Pacific coast of Colombia. Other records: Pacific side of Panama.

Remarks — As far as we know, there were no additional records of P. attenuata since Hartman's original

description, based upon material collected by the Allan Hancock Pacific Expeditions along the Pacific coast of

Colombia and Ecuador.

Material from Pcrlas Islands (Pacific side of Panama), originally referred to Sabellaria (Phragmatopoma)

virgini by MONRO (1933), was correctly ascribed to P. attenuata by Hartman (1944). The original drawing of an

external palea by MONRO (1933, p. 1063) was shown to be slightly misleading by Fauchald (1977), who re¬

examined the material from Perlas Islands and noticed the presence of two distinct teeth on either side of the distal

plumes.

Phragmatopoma peruensis Hartman, 1944

Phragmatopoma peruensis Hartman, 1944: 353, pi. 37. figs 84-85, pi. 39, fig. 99, pi. 41, fig. 104.

Diagnosis (modified from HARTMAN, 1944) — Very small size, less than 10 mm long. Shaft of external paleae

with long, spatulate, distally rounded terminal membrane, strongly curved inward (Fig. Id). Middle paleae with a

conspicuous shoulder at their external edge.

Distribution — Peru.

Remarks — As P. attenuata , P. peruensis seems to be known only from through Hartman’s original

description.

Phragmatopoma virgini Kinberg, 1867

Phragmatopoma virgini Kinberg, 1867: 349. — Kinberg. 1910: 70, pi. 27, fig. 4. — Johansson, 1926: 2, fig.

l(la-b). — JOHANSSON, 1927: 100. — Hartman. 1944: 351, pi. 35. figs 77-78. — 1 1 artmann-Sciikodek, 1962:

155, fig. 202 (as Phragmatopoma c.f. virgini — HARTMAN, 1966: 75, pi. 24, figs 6-8. — RlNGUELET, 1969: 213.-

ORENSANZ, 1974: 55, pro parte.

Source :

212

F. LANA & C. S. BREMEC

Sabellaria macropalea — Pratt, 1901 : 13, pro parte.

Diagnosis — Opercular crown subcircular. External opercular palea with only two main teeth along outer

margins, without any process between them (Fig. le). Middle paleae smooth, very fine and terminating in a hook.

Abdominal uncini with 6 teeth. Maximum reported length 25 mm.

Distribution — Buket Island, San Nicolas Bay, Southern Chile (also spelt Bucket Island by earlier authors,

this site is probably Sanchez Island, according to Hartman, 1966, p. 1); Ramuncho, near Concepcion, Central

Chile; Malvinas-Falkland Islands.

Remarks — P. virgini was originally described from the Strait of Magellan, near Buket Island (= Sanchez

Island), southern Chile. Kinberg (1867) referred to the number and aspect of external paleae ("extemae 66

truncate, spina clongata armatae...") but provided no drawings. Eulers (1901b) re-examined the type material and

considered his species Hermella orbifera (Ehlers, 1901a) a synonym of Sabellaria virgini (Kinberg), since he did

not recognize the name Phragmatopoma. However, in the redescription carried out with complementary

specimens from southern Chile, EHLERS (1901b) figured external opercular paleae with sulcate median processes

(pi. XXIII. fig. 1 1). The type specimen of P. virgini was posteriorly studied by Johansson (1926) and Hartman

(1944). Both described external paleae with only two main teeth along their outer, distal margins, without

dentations or a flange between them. Hartman (1944) explicitly remarked that there was no indication of an

attached flange or other structure along the concave edge. So, die presence of a median process in die external

paleae can be considered a useful diagnostic character to distinguish P. virgini and P. moerchi. Consequently, the

material that EHLERS (1901b) referred to S. virgini belongs in fact to P. moerchi , as already suggested by

Hartman (1944). Orensanz (1974) mentioned P. virgini in a list of magcllanic species, but according to the

provided synonymy he also included earlier findings (EHLERS, 1901a: Monro, 1936) which in fact correspond to

P. moerchi. P. virgini is an intertidal species, known mainly from southern and central Chile. The Malvinas-

Falkland Islands citation (Pratt, 1901; Hartman, 1944) represents its unique record from the Atlantic ocean.

Phragmatopoma moerchi Kinberg, 1867

Phragmatopoma moerchi Kinberg, 1867: 349. — Hartman, 1944: 350,pl. 35, fig. 76, pi. 36, figs 80-83, pi.

39, figs 97-98. — HaRTMANN-SchrOder, 1960: 38. — HARTMANN-SCHRODER, 1962: 154, fig. 201. —

Hartmann-SchrOder. 1965: 304.

Phragmatopoma morchii — JOHANSSON, 1926:4, fig. 1(2-8). — JOHANSSON, 1927: 101.

Hermella orbifera — Ehlers, 1901a: 267.

Sabellaria virgini — EHLERS, 1901b: 199, pi. 23, figs 1-4, 7-12, pi. 24, figs 1-5, pro parte (non KINBERG,

1867).

? Sabellaria (Phragmatopoma) moerchi — Monro. 1936: 171.

Phragmatopoma virgini — ORENSANZ, 1974: 55, pro parte.

Diagnosis — Opercular crown flat and subcircular. External opercular paleae with a rectangular flange, frayed

at the distal end (Fig. If). Middle paleae transversely rugose and slightly roughened on the outer side, terminating

in a hook. Maximum reported length 50 mm.

Distribution — South America: Peru; northern and central coasts of Chile; Patagonia (?). Other records:

Hawaii.

Remarks — P. moerchi is an intertidal and subtidal species, known from Peru to Chile and west to Hawaii.

Sabellaria (Phragmatopoma) moerchi described by Monro (1936) from 43°50' S - 65°0r 51" W (near Dos

Bahias Cape, off Patagonia) could be referred to P. moerchi , since this author found " ... large comb-like processes

...” in die external opercular paleae. This would be die only record of the species in die Atlantic Ocean. However,

MONRO (1936, p. 15) remarked that he could " ... find nodiing significant to distinguish this species from

Johansson's account of Kinberg's Phragmatopoma lapidosa ". We think that this material should be reviewed

before die distribution range of P. moerchi is extended to die Atlantic.

Phragmatopoma lapidosa Kinberg, 1867

Phragmatopoma lapidosa Kinberg, 1867: 349. — JOHANSSON, 1926: 2. — JOHANSSON, 1927: 99. —

Hartman, 1944: 348, pi. 35, figs 73-75, pi. 36, fig. 79, pi. 40, figs 102-103. — Amaral, 1987: 471, figs. 1-5.

? Sabellaria fauveli — Gravier, 1909: 650, pi. 18, figs 60-69.

Source : MNHN. Paris

SABELLARIIDAE FROM SOUTH AMERICA

213

Diagnosis — External paleae witli a long conspicuous pinnate plume arising close to die upper distal margin of

the palea (Fig. lg). Middle paleae strong, uncinate, with a basal tooth. Inner paleae similar, but smaller. Uncini

with 8 teeth. Maximum reported length 23 mm.

Distribution — South America: SE Brazil (from Rio Grande do Sul to Rio de Janeiro, and probably

northward); Peru (?). Ollier sites: Caribbean; Atlantic coast of Mexico; Florida.