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Vol. 26 (1)

REVISTA DE LA

SOCIEDAD ESPAÑOLA DE MALACOLOGÍA

Oviedo, junio 2008

Iberas

Revista de la

Sociedad Española de Malacología

Comité de Redacción (Board of Editors)

Editor di Publicaciones (Editor-in-Chief)

Serge Gofas Universidad de Málaga, España

Director de Redacción (Exkutive Editor )

Gonzalo Rodríguez Casero Apdo. 1 56, Mieres del Camino, Asturias, España

Editora Ejecutiva (Managimg Editor)

Eugenia Mg Martínez Cueto-Felgueroso Apdo. 1 56, Mieres del Camino, Asturias, España

Editores Adjuntos (Associate editors)

Francisco Javier Conde de Saro	Embajada de España, Japón
Benjamín Gómez Moliner	Universidad del País Vasco, Vitoria, España
Ángel Antonio Luque del Villar	Universidad Autónoma de Madrid, Madrid, España
Emilio Rolán Mosquera	Universidad de Vigo, Vigo, España
José Templado González	Museo Nacional de Ciencias Naturales, CSIC, Madrid, España
Jesús S. Troncoso	Universidad de Vigo, Vigo, España
Comité Editorial (Board of Reviewers)
Kepa Altonaga Sustacha	Universidad del País Vasco, Bilbao, España
Eduardo Angulo Pinedo	Universidad del País Vasco, Bilbao, España
Rafael Araujo Armero	Museo Nacional de Ciencias Naturales, Madrid, España
Thierry Backeljau	Instituí Royal des Sciences Naturelles de Belgique, Bruselas, Bélgica
Rüdiger Bieler	The Field Museum, Chicago, Estados Unidos
Sigurd v. Boletzky	Laboratoire Arago, Banyuls-sur-Mer, Francia
José Castillejo Murillo	Universidad de Santiago de Compostela, Santiago de Compostela, España
Karl Edlinger	Naturhistorisches Museum Wien, Viena, Austria
Antonio M. de Frías Martins	Universidade dos Acores, Acores, Portugal
José Carlos García Gómez	Universidad de Sevilla, Sevilla, España
Gonzalo Giribet de Sebastián	Harvard University, EE.UU.
Edmund Gittenberger	National Natuurhistorisch Museum, Leiden, Holanda
Ángel Guerra Sierra	Instituto de Investigaciones Marinas, CSIC, Vigo, España
Gerhard Haszprunar	Zoologische Staatssammlung München, München, Alemania
Yuri 1. Kantor	A.N. Severtzov Institute of Ecology and Evolution, Moscú, Rusia
María Yolanda Manga González	Estación Agrícola Experimental, CSIC, León, España
Jordi Martinell Callico	Universidad de Barcelona, Barcelona, España
Ron K. O'Dor	Dalhousie University, Halifax, Cañada
Takashi Okutani	Nihon University, Fujisawa City, Japón
Marco Oliverio	Universitá di Roma "La Sapienza", Roma, Italia
Pablo E. Penchaszadeh	Museo Argentino de Ciencias Naturales "Bernardino Rivadavia", Buenos Aires, Argentina
Winston F. Ponder	Australian Museum, Sydney, Australia
Carlos Enrique Prieto Sierra	Universidad del País Vasco, Bilbao, España
M^ de los Ángeles Ramos Sánchez	Museo Nacional de Ciencias Naturales, CSIC, Madrid, España
Francisco Javier Rocha Valdés	Instituto de Investigaciones Marinas, CSIC, Vigo, España
Paul G. Rodhouse	British Antarctic Survey, Cambridge, Reino Unido
Joandoménec Ros i Aragonés	Universidad de Barcelona, Barcelona, España
María Carmen Salas Casanovas	Universidad de Málaga, Málaga, España
Gerhard Steiner	Instituí für Zoologie der Universitát Wien, Viena, Austria
Victoriano Urgorri Carrasco	Universidad de Santiago de Compostela, Santiago de Compostela, España
Anders Warén	Swedish Museum of Natural History, Estocolmo, Suecia
Portada de Iberus

Iberus gualtieranus (Linnaeus, 1758), una especie emblemática de la península Ibérica, que da nombre a la revista. Dibujo realizado por José Luis González Rebollar “Toza”.

Iberus

REVISTA DE LA

SOCIEDAD ESPAÑOLA DE MALACOLOGÍA

Vol. 26 (1)

Oviedo, junio 2008

Iberus

Revista de la

Sociedad Española de Malacología

Iberus publica trabajos que traten sobre cualquier aspecto relacionado con la Malacología. Se admiten también notas breves. Iberus edita un volumen anual que se compone de dos o más números.

Instrucciones para los autores

Los manuscritos deben remitirse a: Serge Gofas, Editor de Publicaciones, Departamento de Bio- logía Animal, Universidad de Málaga, Campus de Teatinos, s/n, 29071, Málaga, España.

Los trabajos se entregarán por triplicado (original y dos copias). Se recomienda a los autores leer cuidadosamente las normas de publicación que se incluyen en cada número de la revista.

SUBCRIPCIONES

Iberus puede recibirse siendo socio de la Sociedad Española de Malacología, en cualquiera de sus formas, o mediante intercambio. Aquellos socios que deseen adquirir números atrasados deberán diri- girse al bibliotecario.

Los no socios deberán ponerse en contacto con BACKHUYS PUBLISHERS, P.O. Box 321, 2300 AH Leiden, The Netherlands. Tel.: +31-71-31 70 208, Fax: +31-71-31 71 856, Correo Elec- trónico: backhuys@euronet.nl

Los resúmenes de los artículos editados en esta revista se publican en Aquatic Science and Fisheries Abstracts (ASFA) y en el Zoological Records, BIOSIS.

Contents list published in Aquatic Science and Fisheries Abstracts and Zoological Records , BIOSIS.

Dep. Leg. B-43072-81 ISSN 0212-3010

Diseño y maquetación: Gonzalo Rodríguez Impresión: LOREDO, S. L. - Gijón

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Re-discovery of living specimens of Heliacus ( Gyriscus ) jef- freysianus (Tiberi, 1867) (Gastropoda: Architectonicidae)

Redescubrimiento de ejemplares vivos de Heliacus ( Gyriscus ) jef- Jreysian i/s (Ti be ri , 1867) (Gastropoda: Architectonicidae)

Constantine MIFSUD* and Panayotis OVALIS**

Recibido el 17-VII-2007. Aceptado 9-X-2007

ABSTRACT

Heliacus (Gyriscus) ¡effreysianus (Tiberi, 1 867), a rare architectonicid species associated with Corallium rubrum (L., 1758), has been rediscovered alive off Crete, eastern Mediter- ranean.

RESUMEN

Heliacus ( Gyriscus ) ¡effreysianus (Tiberi, 1 867), una especia rara de architectonicido aso- ciado a Corallium rubrum (Linnaeus, 1 758), ha sido redescubierta con ejemplares vivos, frente a la isla de Creta en el Mediterráneo oriental.

KEY WORDS: Mollusca, Gastropoda, Architectonicidae, Heliacus j effreysianus, Crete. PALABRAS CLAVE: Mollusca, Gastropoda, Architectonicidae, Heliacus jeffreysianus, Creta.

INTRODUCTION

Heliacus ( Gyriscus ) jeffreysianus was described by Tiberi (1867) from three specimens collected from a red coral substratum off Sardinia. He described the species a year after its discovery, as stated by Coen (1932).

SYSTEMATICS

Original description: Cochlea turbinata, elato-conica, turrita, modice umbilicata, inteo- fulvescens; apex obtusiusculus, laevigatus, vértice intorto, subperf orato, spiraliter invo- luto; anfr. 7 convexi, sutura profunda divisim transverse cingulati, cingulis confortis, alter- natim majoribus (num.fere 15 totidemque

minaribus in ultima anfractu; num. 6 in penúltimo), eleganter granulosis, submonili- formibus; anfr. Ultimus rotundatus, subin- flatus, basi paululum depressus; umbilicus mediocris, pervius, superne circolariter crenu- latus; apert. Subcircularis, effusa, intus haud margaritacea, marginibus acutis, callo pari- etali junctis; margine columellari sinuato, reflexo, umbilici partem occultante. - Diam. Maj. 9, min. 8, alt 10? mili. - Operculum corneum, superne núcleo centrali depresso lamellaque erecto-crenulata multispiratum, inferné processu centrali styliformi paucispi- rato praeditum, limbo peripherico incrassa- tum- Animal hucusque incognitum.

Hab. Infundís coralligenis maris Sar- diniam meridionalem ambientis.

* 5, Triq ir-Rghajja, Rabat RBT 2486, Malta

** Agisilaou 37-39, Tzitzifies/Kallithea, 17674 Athens, Greece

1

Iberus , 26 (1), 2008

Figure 1. Heliacus (Gyriscus) jeffreysianus (Tiberi, 1867), off Crete Island on Corallium rubrum (Linnaeus, 1758) in 120m. Size: 9x8 mm. Photo P. Ovalis.

Figura 1. Heliacus (Gyriscus) jeffreysianus (Tiberi, 1867), frente a la isla de Creta sobre Corallium rubrum (Linnaeus, 1758) en 120m. Size: 9x8 mm. Foto P. Ovalis.

Tiberi dedicated his species to the illustrious malacologist John Gwyn Jef- freys (1809-1885). Two of the specimens are presently in the Coen collection at The Hebrew University, (Department of Zoology) Jerusalem, Israel and the other specimen is in the Jeffreys collection at the Smithsonian Institution, Washington (USA) (Melone and Taviani 1984).

New material: Two live specimens of Heliacus ( Gyriscus ) jeffreysianus were recently recovered from a living colony of Corallium rubrum (Linnaeus, 1758) from off the island of Crete at a depth of 120 m. Figure 1 shows one of the two similar specimens, measuring h= 9 mm x w= 8 mm which is about the same size as those found by Tiberi. The specimens were hand picked from a coral colony by a professional scuba diver from Crete using specialized diving equipment. It is not known whether the molluscs were actually feeding on the coral polyps. However, the species seems to have a cióse connection with C. rubrum. Several species from the family Architectonici- dae are known to be parasitic on coráis (Bieler 1993). Judging from the two presently known records, the species has always been found with these red coráis, and as it is well known, it was never found in any other Mediterranean habitat notwithstanding the large amount of research carried out in the last hundred years.

Since its original description, the species had never been found again until recently, when living specimens of Heliacus jeffreysianus were collected in the Adriatic Sea (Stanic and Schiapar- elli, 2007). It is very curious, but not surprising, that both this and our dis- coveries were recorded at the same time and at distantly separated places. This is certainly due to the more recent interest being undertaken both by amateur and professional researchers in the depths of the red and white coral substratum of the Mediterranean Sea. The authors are also aware of other unrecorded species living in this part of the Mediterranean, and originally described from deep water in the Atlantic.

Otherwise, Heliacus jeffreysianus has only been cited in the literature in a few species lists and catalogues pertaining to the Mediterranean malacofauna and it was even thought to be extinct. More- over, no fossil specimens of the species have ever come to light (Melone and Taviani 1984).

Monteros ato (1880) had com- mented about the species of Tiberi "II G. jeffreysianus, é una delle nostre piú rare gemme, la cui scoperta, come di tante altre raritá coralligene, si deve al Dr. Tiberi. Soltanto tre esemplari ne sono conosciuti sinora. Beati possidentes! lo voglio ammettere che nella mente di un naturalista il Gyriscus abbia piú valore

2

Mifsud AND OvaliS: Re-discovery of living specimens of Heliacus (Gyriscus) jeffreysianus

Figure 2. Map of the Mediterranean showing the three locadons cited for H. jeffreysianus. 1: Sardi- nia Island; 2: Adriatic Sea; 3: Crete Island.

Figura 2. Mapa del Mediterráneo mostrando las tres localidades citadas para H. jeffreysianus. 1: isla de Cerdeña; 2: mar Adriático; 3: isla de Creta.

del piú grosso diamente della corona d'Inghilterra, ma francamente il prezzo al quale lo vende il Dr. Tiberi, per una conchiglia cosí piccola, sará riguardato tanto dai naturalisti quanto dai mercanti come assai esagerato"

In transía tion: "The G. jeffreysianus is one of our most rare gems, its discovery, like many other coralligeneous rarities, is owed to Dr. Tiberi. Only thee speci- mens are known up to now. Blessed are the possessors\ I must admit that in the minds of the naturalist the Gyriscus has more valué than the largest diamond from the British crown, but frankly the price which Dr. Tiberi has asked, for such a small shell is regarded by natu- ralists and also by merchants as being exaggerated."

H. jeffreysianus is one of the most beautiful species from the family Archi- tectonicidae. Its sculpture of small- beaded spiral chords and its trochoid shape make it outstanding and very dis- tinguished among the other species of the family in the Mediterranean. In fact, Tiberi (1867) created a genus for it, Gyriscus, which is nowadays a subgenus of Heliacus. A very similar Pacific species is H. ( Gyriscus ) asteleformis (Powell, 1965) from New Zealand.

Coen (1932) figured the operculum from one of the two specimens in his collection (also figured in Melone and Taviani, 1984). Melone and Taviani (1984) described and figured a syntype

from the Coen collection. They also figured the radula (as redrawn after Merril, 1970). Other descriptions and diagnoses of the genus and the species can also be found in Coen (1932), Melone and Taviani (1984) and in Bieler (1993).

CONCLUSIONS

This very long elapsed period of o ver 140 years for the re-discovery for H. jeffreysianus is in all probability due to its rarity and the very particularly restricted and difficult to sample habitat. Red coral was traditionally har- vested by fishermen utilizing a particu- lar gear called the Cross, which consists of two large beams tied together in the form of a cross and armed with dan- gling ropes and pieces of netting to enable the coral to entangle during dredging. This heavy equipment, although it seemed adequate for the purpose, besides being very destructive to the substratum, constantly shakes the entangled coráis and the molluscs seem to always fall off before the gear is brought aboard the vessel. The modern method of manual harvesting through SCUBA is more selective, and therefore much less destructive. However, it is much more risky and dangerous.

Curiously, this species had not been discovered on red coral before, although

3

Iberus , 26 (1), 2008

the method of manual harvesting of coral by specialized deep diving equipment (using a mixture of gases) has now been in practice for many years, especially by Spanish, Italian and Greek coral divers. More probably, it may take the keen eyes of a biologist, a naturalist or a shell col- lector to notice and pick out the small mollusc shells in situ. Therefore any spec- imens brought up by chance by the fish- ermen or the divers are probably either thrown back into the sea with the other rubbish as in the case of the fishermen or in the case of the diver, they fall off the coral unnoticed during the long decom- pression process. Moreover, the diver would be even more concerned for his "treasure" rather than a few "worthless" shells. Although Mediterranean Corallium rubrum is also found at great depths in the Mediterranean, the two existing records of H. jeffreysianus are both from shallow

BIBLIOGRAPHY

Bieler, R., 1993. Architectonicidae ofthe Indo-Pa- cific. Gustav Fischer Verlag, pp. 377. Stuttgart. Coen, G. S., 1932. Sul genere Gyriscus, Tiberi, 1867. Bollettino della Societd Veneziana di Scienze Naturali, 1 (1): 9-13.

Melone, G. and Taviani, M., 1984. Revisione delle Architectonicidae del Mediterráneo. Atti del Simposio: Sistemática dei Prosobranchi del Mediterráneo, Bologna 24-26 Setiembre 1992, (B. Sabelli, ed.) Lavori S.I.M., 21: 149-192. Merrill, A. S., 1970. The family Architectonici- dae (Gastropoda: Mollusca) in the western and eastern Atlantic. Unpubl. Ph.D. Thesis, Univ. Delaware (Univ. Microfilms Int. Inc., Ann Arbor, Michigan, U.S.A., Nr. 7144444).

water living colonies. Stanic and Schia- parelli (2007) did not mention the species on which they found their specimens. Finally, this record extends the species dis- tribution to quite a larger area of the Mediterranean (Fig. 2) and it is expected that more specimens which could con- tribute to the study of the biology of the species are likely to turn up.

ACKNOWLEDGEMENTS

We would like to thank Agios Nico- laos, a specialized deep sea coral diver for donating one of the two specimens which he collected to one of the authors (P. O.) for this study. Thanks are also due to Sophie Valtat (Belgium) for pro- viding important literature and to S. Gofas (Spain) for revising and enhanc- ing the manuscript.

Monterosato, T. A., 1880, Nota sopra alcune conchiglie coralligene del Mediterráneo. Bol- lettino della Societd Malacologica Italiana, 6: 243-259.

Stanic, R. and Schiaparelli, S., 2007. New finding of living specimens of the rare ar- chitectonicid Heliacus (Gyriscus) jeffreysianus (Tiberi, 1867). Bollettino Malacologico, 43 (9-12): 143-146.

Tiberi, N., 1867. Diagnose du nouveau genre méditerranéen Gyriscus. Journal de Conchy- liology, 15: 303. Paris.

4

Notes on West African Perrona (Gastropoda: Clavatulidae), with the description of a new species

Notas sobre Perrona (Gastropoda: Clavatulidae) en Africa

Occidental, con la descripción de una nueva especie

Emilio ROLÁN*, Peter RYALL** and Juan HORRO***

Recibido el 31 -VI 1-2007. Aceptado el 19-X-2007

ABSTRACT

The type species of the genus Perrona is poorly known and given an erroneous type local- ity. One of the purposes of this paper is to clarify its status and correct spelling as well as illustrating the species and defining its distribution area. A new species from Angola belonging to this genus is described. The shell, protoconch, operculum and radula are illustrated, and the reasons for assigning this new species to this genus are discussed. All known species of Perrona are figured.

RESUMEN

La especie tipo del género Perrona es poco conocida y la localidad tipo dada es errónea. El objetivo de este trabajo es clarificar su situación, su correcto nombre, además de repre- sentar la especie y clarificar su área de distribución. Se describe una nueva especie de este género de Angola. Se muestran concha, protoconcha, opérculo y rádula de la nueva especie y se discuten las razones para asignarla a este género y no a otros con similar morfología. Se ilustran todas las especies conocidas de este género.

KEY WORDS: Clavatulidae, Perrona, West Africa, Angola, new species.

PALABRAS CLAVE: Clavatulidae, Perrona, África occidental, Angola, nueva especie.

INTRODUCTION

Classical malacological works like Bruguiére (1792), Lamarck (1801, 1816 and 1822), Kiener (1840) and Reeve (1843, 1845) and publications dealing with Turridae (s.l.) such as Récluz (1851), Petit de la Saussaye (1851), von Maltzan (1883, 1884), Sykes (1905), Dautzenberg (1912), Strebel (1912, 1914) have described numerous West African species assigned to the family Clavatulidae Gray, 1853.

Their generic placements and syn- onymies are still not clear. Some modem works like Knudsen (1952, 1956), Ardovini (2004), Boyer and Hernán- dez (2004), Nolf (2006), Nolf and Ver- straeten (2006) and Boyer and Ryall (2006) have described new species or revised others, placing most of them in the genus Clavatula.

Among our material from Angola, dredged over many years by Xico Fer-

* Museo de Historia Natural, Campus Universitario Sur, E 15782 Santiago de Compostela, Spain

** St. Ulrich 16, A-9161 Maria Rain, Austria

*** Montero Ríos, 30-3° 36201 Vigo, Spain

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Iberas, 26 (1), 2008

nandes, a new small unidentified species was found. Its description is one of the subjects of this work. The generic attribution to the genus Perrona (Schu- macher, 1817) requires a review of the type species because it is a rather poorly known species. This paper therefore also comments on the type species.

The identity of Perrona perron

Martini and Chemnitz (1788: 278, pl. 164, figs. 1573, 1574) illustrated a shell they named "Der Perron ". Later Gmelin (1791), referring to Chemnitz's figures, described it as Murex perron and indicated "in Océano australi" as its geographic origin. This type locality is obviously wrong. These figures, or the shell they represent, can be considered to be the lectotype. Its present where- abouts, as noted below, are unknown.

When Lamarck (1816) described Pleurotoma spirata he also made refer- ence to the same illustrations, but sepa- rated his species from them by stating "La figure citée de Chemnitz offre sur la base du dernier tour ; des sillons dont notre coquille est absolutement dépourvue".

Schumacher (1817) also referred to the same illustrations of Chemnitz when he described the genus Perrona and nomi- nated Perrona tritonium as the type of this genus. P. tritonium is therefore a júnior objective synonym of Perrona perron (Gmelin). Again no locality was given.

The species was subsequently described for a third time by Reeve (1843) who referred once more to Chemnitz's illustrations. He gave it the ñame Pleuro- toma perronii, drawing his own figure from his own shell. He likewise did not State a locality or habitat. Reeve cited Lamarck 's spirata as a different species, writing "1 have a shell before me ofvery dif- ferent character (Pleurotoma Perronii, nobis), answering exactly to the figure in question". Reeve (1843) did not cite Gmelin and therefore appeared to con- sider his ñame as a valid new species. However it is clearly a júnior synonym of Gmelin's species and it is concluded that this was an omission in Reeve's work.

Marrat (1877) was the first to give an indication of the true range of the

species when he included it in a list of North-west African shells which he stated carne "from Madeira to the Gulf of Guinea".

Tryon (1884), although stating his Opinión that this species was an inter- medíate form between lineata and spirata , mentioned it as Clavatula (sub- genus Perrona ) perron Chemnitz and provided a detailed description.

Strebel (1912), in his revisión of genus Perrona, treated as clearly differ- ent species both spirata and perron. He was able to examine Chemnitz's speci- men from which the famous drawings were made and reillustrated it. He referred immature specimens of the species to Reeve's description, calling them perron var. reevei. He also correctly indicated part of the correct habitat range of the species, citing specimens he had examined from Pointe Noire, Congo to Ambriz, northem Angola.

Knudsen (1952) employed the ñame "Clavatula perronii (Reeve)" noting that the "Atlantide expedition" could not obtain any additional material and that Chemnitz's type could no longer be traced at the ZMUC.

Powell (1966), who referred cor- rectly to the type species of Perrona, did not figure Perrona perron but illustrated Perrona spirata (Lamarck, 1816).

More recently, Cernohorsky (1974) figured a syntype from Chemnitz (in ZMUC), commenting that "the species most probably Uves in West Africa but this locality has been not substantiated by either literature records or authentic specimens. Another possibility is that Murex perron is conspecific with Pleurotoma spirata Lamarck, 1816, as suggested by Nordsieck (1968: 154) although the two species appear quite distinct".

Finally, Bernard (1984, fig. 182) figured under the erroneous ñame "Clavatula kraepelini" three specimens of this species. He unknowingly extended Strebel's habitat range northwards, quoting the localities of both Cape Este- rias and Mayumba in Gabon, and indi- cating a depth of -20 to -50 meters.

After examining Reeve's type speci- men, the available literature and some

ó

RoláN ET AL.: Notes on West African Perrona with the description of a new species

shells in the collection of one of the authors (PR), it was decided to record some additional information about this poorly known group.

Abbreviations:

AMNH American Museum of Natural History, New York

ANSP Academy of Natural Sciences, Philadelphia

BMNH The Natural History Museum, London

MCZ Museum of Comparative Zoology, Harvard university

MHNS Museo de Historia Natural "Luis Iglesias" Universidad, Santiago de Compostela

MNCN Museo Nacional de Ciencias Naturales, Madrid

MNHN Muséum national d'Histoire naturelle, París

ZMUC Zoologisk Museum, Copenhagen USNM National Museum of Natural History, Washington ZSM Zoological Staatmuenchen Museum, Muenchen CJH collection of Juan Horro, Vigo CPR collection of Peter Ryall, Maria Rain

SYSTEM ATIC PART

Family Clavatulidae Gray, 1853 Genus Perrona Schumacher, 1817

Type species: Perrona tritonium Schumacher, 1817 = Murex perron Gmelin, 1791 = Pleurotoma perronii Reeve, 1843.

Perrona perron (Gmelin, 1791) (Figs. 1-13)

Der Perron Martini and Chemnitz, 1788: 278, pl. 164. figs. 1573, 1574 (Fig. 1). Murex perron Gmelin, 1971: 3559.

Perrona tritonium Schumacher, 1817: 218.

Pleurotoma perronii Reeve, 1843: pl. 11, sp. 94 (Fig. 2).

Type material: Figured syntype of Der Perron, whereabouts presently unknown; this specimen is reported as examined by Strebel (1912) but could not be traced by Knudsen (1952) who never- theless mentions another shell labelled in the handwriting of Chemnitz. Pleurotoma perronii: holo- type BMNH 1900.2.8.26.

Other material examined: 8 shells (Figs. 4-10), Pointe Noire, Congo (CPR).

Type locality: Erroneous for Der Perron (in Océano australi). Not mentioned in the original descrip- tion of any of the other taxa. Here designated at Pointe Noire, Congo.

Description: Shell (Figs. 3-12) see the original descriptions as well as Tryon (1884) and Strebel (1912). The follow- ing data can be added: the protoconch (Fig. 13) consists of about 2 1 ¡i shiny, smooth whorls, honey brown in colour; the first whorl slightly darker and of 750 pm diameter. From the protoconch whorls a series of opisthocline axial ribs start to form, first as thin riblets extend- ing from the top to the bottom of the whorl, becoming stronger and shaped as an inverted C in the second teleo- conch whorl where their bases become

more globose. Between them small striae can be seen. In the subsequent whorl they detach themselves entirely from the upper subsutural cord which also increases in prominence. In the fourth teleoconch whorl these vestiges of the axial ribs become closer and closer to the lower suture, declining in prominence until they entirely disap- pear. The following whorls are smooth with an irregular, raised subsutural collar and the whorls are traversed by s- shaped striae. At the same time as the axial riblets form in the third whorl.

7

Iberus , 26 (1), 2008

about 9 radial striae also start to emerge becoming slightly stronger in the fol- lowing whorls but then decreasing in intensity in the fourth or fifth whorls and thereafter are hardly noticeable.

The shell is a light honey-brown throughout. On the fourth whorl the subsutural colar starts to become lighter, being entirely white in the fifth whorl. In subsequent whorls it can be interrup- ted by patches of light brown; in the final whorl the two major cords are white interspaced with small brown patches the same colour as the whorl itself and the cords on the columnella are also white.

Size : the shell can reach up to 37.2 mm (Bernard, 1984).

Remarks : The comparison of juvenile specimens of P. perron with species of the genus Clavatula (type species: Clavat- ula coronata Lamarck, 1801) show much similarity in the aspect of the opistho- cline axial ribs, which tend to disappear with maturity in the subsequent whorls. For this reason it is concluded that there is a stronger relationship between these two genera, than with other genera within this family.

Whilst some authors synonymized P. perron with P spirata Lamarck, 1816 it must be noted that not only are they morphologically different, but the latter inhabits an area further to the south, being restricted to the Luanda area where it has been found at -5/50 meters.

Distribution : This species inhabits the West African infralittoral coast from Cap Esterias (Gabon) to Ambriz (northern Angola).

Special remarks: The type locality is always related with a holotype or a lec- totype. In the present case, the original figures are sufficient to determine the identity of the species and it is not nec- essary to designate a neotype; Pleuro- toma perronii was described lacking type locality as confirmed by the label of this holotype in BMNH. If the type locality of the first description is erroneous, and no other is mentioned in the description of the synonymized taxa, it is necessary to give more detailed information. Pointe Noire (Congo) is designated as the type locality being in the center of the known distribution area, as well as a locality mentioned by Strebel (1912) and the source of our specimens. Our material agrees very well with the figures and the known holotype.

Concerning the correct spelling for the ñame of this species, it must be perron, which is the first ñame employed by Gmelin (1791) and which is appa- rently a ñame not dedicated to a person. Tryon (1884) stated that Chemnitz employed the common Dutch ñame "perron" (= flight of stairs, in reference to the profile) and that Reeve (1843), misinterpriting Chemnitz's ñame to be a personal ñame, Latinized it to read "perronii”.

Perrona micro spec. nov. (Figs. 14-19, 21, 23, 24-28)

Material examined: Holotype (Figs. 14, 15), in MNCN (15.05/47050). Paratypes in the following collections: MNHN (1, Fig. 16); BMNH (1, Fig. 17); AMNH (1); USNM (1); ZSM (1); ANSP (1); MCZ (1); CPR (11); CJH (6); MHNS (16, Fig. 18).

Type locality: Palmeirinhas, south of Luanda, Angola, between 3 and 20 meters depth. Etymology: The specific ñame refers to the small size of the species.

Description: Shell (Figs. 14-18) small for the genus, very solid, lanceolate. Protoconch (Figs. 21, 23, 24-26) with a little more than one whorl, of 530 pm in diameter and white in colour. The teleo- conch begins with three grooves that sepárate 4 cords, later increasing to four and then five spiral grooves; there are

six in the subsequent whorl; the two cords immediately below the suture as well as the lowest cord are more promi- nent. This gives the middle part of the whorl a concave appearance whilst the upper and lower parts protrude before their separation at the suture. There is no axial sculpture except for growth

8

RoláN ET AL.: Notes on West African Perrona with the description of a new species

Figures 1-13. Perrona perron. 1: figure from MARTINI AND CHEMNITZ (1788); 2: figure of the holotype of Pleurotoma perronii from Reeve (1843); 3: holotype (see below Figs. 11, 12) of Pleuro- toma perronii (BMNH) at the same comparative size; 4-6: shell (27.6 mm), Pointe Noire, Congo (CPR); 7: shell, 28.6 mm, Pointe Noire (CPR); 8, 9: juveniles, 18.6 and 14.2 mm, Pointe Noire (CPR); 10: shell, 27.2 mm, Pointe Noire (CPR); 11, 12: holotype of P. perronii , 25 mm (BMNH); 13: spire and protoconch, Pointe Noire (CPR).

Figuras 1-13. Perrona perron. 1: figura de MARTINI Y CHEMNITZ ( 1 788); 2: figura del holotipo de Pleurotoma perronii, de Reeve ( 1 843); 3: holotype ( véase abajo Figs. 1 1, 12) de Pleurotoma perronii (BMNH) con el mismo tamaño relativo; 4-6: concha, 27,6 mm, Pointe Noire, Congo (CPR); 7: concha, 28,6 mm, Pointe Noire (CPR); 8, 9: juveniles, 18,6 y 14,2 mm, Pointe Noire (CPR); 10: concha, 27,2 mm, Pointe Noire (CPR); 11, 12: holotipo de P. perronii, 25 mm (BMNH); 13: spire and protoconch, Pointe Noire (CPR).

9

Iberus, 26 (1), 2008

Figures 14-19. Perrona micro spec. nov. 14, 15: holotype, 10.3 mm (MNCN); 16: paratype, 10.6 mm (MNHN); 17: paratype, 8.5 mm (BMNH); 18: paratype, 7.6 mm (scanning electrón micro- scope) (MHNS); 19: operculum (SEM). Figures 20-23. Comparison of the spire and protoconch of Clavatula quinteni (Figs. 20, 22) and Perrona micro (Figs. 21, 23).

Figuras 14-19. Perrona micro spec. nov. 14, 15: holotipo, 10,3 mm (MNCN); 16: paratipo, 10,6 mm (MNHN); 17: paratipo, 8,5 mm (BMNH); 18: paratipo, 7,6 mm (microscopio electrónico de barrido) (MHNS); 19: opérenlo ( MEB). Figuras 20-23. Comparación de la espira y protoconcha de Clavatula quinteni (Figs. 20, 22) y Perrona micro (Figs. 21, 23).

10

ROLÁN ETAL.: Notes on West African Perrona with the description of a new species

Figures 24-27. Perrona micro. 24: detail of the spire; 25, 26: detail of the protoconch; 27: radular tooth; 28: radula. Figures 29-33. Perrona obesa. 29: holotype, 34.0 mm (BMNH); 30: shell, 31.2 mm, 10 m, Namibe, Angola (CER); 31: shell, 35.7 mm, Namibe, Angola (CPR); 32, 33: shells, 40.2, 41.6 mm, Sacomar, Namibe, Angola (CPR).

Figuras 24-27. Perrona micro. 24: detalle de la espira; 25, 26: detalle de la protoconcha; 27: dientes de la rádula; 28: rádula. Figuras 29-33. Perrona obesa. 29: holotipo, 34. 0 mm (BMNH); 30: concha, 31,2 mm, 10 m, Namibe, Angola (CER); 31: concha, 35,7 mm, Namibe, Angola (CPR); 32, 33: conchas, 40.2, 41.6 mm, Sacomar, Namibe, Angola (CPR).

Iberus, 26 (1), 2008

lines which form an U-shape in the concave central portion; this is reversed on both the upper and lower protruding parts forming an overall S-shape on the whorl. There are about 6 whorls on the teleoconch, increasing gradually in width and height. The last whorl becomes elongated towards the base, the siphonal canal is widely open and almost similar in length to the lowest part of outer lip. The aperture is ovoid, with an U-shape sinus in the upper part, a sharp external lip, and a small callus on the columella. There are 20 spiral grooves from the periphery to the base. The colour is typically light brown or orangish, with white and dark blotches alternating on the subsutural cords, but in a few specimens the colour is darker and the white pattern is absent.

Soft parts: Study of a retracted speci- men preserved in alcohol reveáis a light coloured animal; the operculum (Fig. 19) is ovoid with the nucleus centrally placed on the interior. The radula (Fig. 28) is formed by two rows of about 70 elongate and sharply pointed marginal teeth (Fig. 27) at the center of which is a very small central tooth reduced to a cusp.

Dimensions : Flolotype is 10.3 mm. The largest paratype is 12 mm.

Distribution: Only known from the type locality, where it is probably endemic.

Discussion: There is no known species from West Africa with which it can be confused. Only juvenile forms of Clavatula quinteni Nolf and Verstraeten, 2006, which are much larger when adult, are similar in profile and coloura- tion; they both lack axial sculpture (see comparison in Figs. 20 and 21, 22 and 23) but C. quinteni has a much more elongated siphonal canal, a larger proto- conch (more than double the diameter) and lacks spiral grooves.

There was some hesitation about the generic assignment of this new species. Comparison with morphologically similar species in some genera was made, in particular Microdrillia Casey, 1903; Suavodrillia Dalí, 1918; Parecuneus Laseron, 1954, and Maoritomella Powell,

1942, Tomopleura Casey, 1904, and Viridi- turris Powell, 1964. In all cases opercu- lum and radula do not agree.

Perrona micro spec. nov., in spite of its small size, belongs to Clavatulidae. This is confirmed by the operculum with a medium-lateral nucleus and the wishbone-like marginal teeth with a vestigial rachidian one in the middle.

Powell (1966) reviewed the Turri- dae (s. 1.) and defined the subfamily Clavatulinae H. and A. Adams, 1858 with four recent and two fossil genera; the recent genera being Clionella, Clavat- ula, Perrona (with subgenus Tomellana) and Pusionella. Kilburn (1985), who dealt only with South African species, noted 4 genera; Toxiclionella, Bentho- clionella , Clavatula and Clionella. Tucker (2004) considers 492 fossil and 97 recent species in this group. Later Bouchet and Rocroi (2005) elevated Clavatuli- dae to family status.

The genus Clavatula Lamarck, 1801 is relatively abundant along the West Africa coast. Powell (1966) mentions 11 species. Most of them, including the type species ( Clavatula coronata Lamarck, 1801) are of large size. Other species recently illustrated and/or described, as detailed in our introduction, are also rel- atively large. Although Boyer and Ryall (2006) noted that Knudsen (1952, 1956) classified other genera of Clavatul- idae under the genus Clavatula, subse- quent authors seem to ignore these genera and their paramaters as estab- lished by Kilburn (1985). A revisión could conclude that some of them belong to other genera.

The genus Clavatula is described by Powell (1966): "shell modera tely large to large sized, 15 - 55 mm, very solid, buccinoid, coarsely axially and spirally sculptured; with a tall, often coronated spire, and a trúncate body-whorl, termi- nated in a relatively short reflected and deeply notched anterior canal.... Oper- culum ovate-lunate with a medio-lateral nucleus. Radula consisting of a pair of stout narrowly pointed marginal teeth of modified wishbone type, the proxi- mal extremity sepárate and superim- posed upon the larger element. A small

12

RoláN ET AL. : Notes on West African Perrona with the description of a new species

Figures 34-37. Perrona spirata. 34-36: shell covered by organic material, 31.5 mm, Luanda, Angola (CPR); 37: operculum. Figures 38-41. Perrona subspirata. 38: shell, 31.5 mm; 39-41: shell, 32.0 mm, Namibe, Angola (CPR); 42: operculum.

Figuras 34-37. Perrona spirata. 34-36: concha recubierta por material orgánico, 31,5 mm, Luanda, Angola (CPR); 37: opérculo. Figuras 38-41. Perrona subspirata. 38: concha, 31,5 mm; 39-41: concha, 32,0 mm, Namibe, Angola (CPR); 42: opérculo.

13

Iberus, 26 (1), 2008

but we 11 formed unicuspid central tooth is present also." According to Kilburn (1985) the main features of Clavatula are: deep anal sinus, realtively long siphonal canal, distict parietal tubercle and proto- conch that is bluntly domed with about 2 1/2 whorls.

The species P. micro spec. nov. has some shell characters of Clavatula but has no axial sculpture and is smaller than all of them. Clavatula cossignanii Ardovini, 2004, the smallest Clavatuli- dae known in West Africa, is different in most features including the fewer number of protoconch whorls and is endemic to Senegal. The holotype is 13.2 mm but it can reach a size of 15.9 mm (CPR).

According to Powell (1966) the genus Clionella Gray, 1847 differs from Pusionella Lamarck, 1801 by its clavi- form shape with tall, flat-sided spire whorls; simple long flexuous axials ribs without either subsutural or peripheral processes and a truncated body-whorl. Kilburn (1985) defines Clionella with an anal sinus; a slight notch; siphonal canal short with no distinct parietal tubercle; protoconch somewhat conical, of about 2 whorls, the first one rounded and tilted. The genus is usually restricted to South Africa. P. micro spec. nov. lacks axial sculpture, its sinus is deep and does not have a truncated body-whorl: therefore it does not agree with Clionella.

The new species was also ruled out of the genus Pusionella Gray 1847 because many specific characters are absent in P. micro ; the flat-sided whorls; the outer lip bordered by a broad, sub- sutural, very slight sinus and the smooth and polished surface.

Finally, the genus Perrona Schu- macher, 1817 is described by Powell (1966) as: "shell moderately large, 25 - 40 mm, rather narrowly fusiform, with a tall spire of rapidly increasing whorls

ACKNOWLEDGEMENTS

The authors wish to thank the Euro- pean Synthesys Program which allowed one of the authors (ER) to examine the

and a narrow body-whorl... surface smooth, or nearly so... with a conspicu- ous narrowly carinate subsutural collar.... operculum as in Clavatula... radula with a pair of elongate margináis and a narrow-based unicusp central tooth."

The known West African species of Perrona, all figured in the plates in the present work, are the following: P. perron (Gmelin, 1791) (Figs. 1-13), P. spirata (Lamarck, 1816) (Figs. 34-37), both already mentioned, P. obesa (Reeve, 1843) (Figs. 29-33) and P subspi- rata (von Martens, 1903) (Figs. 38-41), both endemic to South Angola. Other authors have placed other species in this genus, for example Perrona nifat (Bruguiére, 1789) by Abbott and Dance (1986), but this generic place- ment is erroneous in our opinión. Powell (1966) also mentions another West African species belonging to this genus but placed in the subgenus Tomellana Wenz, 1843: Perrona ( Tomel - lana) lineata Lamarck, 1816; but this shell has a short, concave-outlined spire and a deep slit-like anal sinus and does not resemble our species. Strebel (1912) referred other species to Tomel- lana; they also do not correspond with the species currently reviewed.

Perrona micro spec. nov. is more similar to Perrona perron than to any other type species and the new species is placed in this genus as being the closest. Also noticed is a similarity in the colouration of the subsutural cord as well as the S-shaped axial striae. We find this at present the better solution rather than to create a new genus.

Whilst the similarity noted with Clavatula quinteni should not create con- fusión, a result of this paper must also be to assign this species to the genus Perrona although this has not been the reason for this work.

type material of Pleurotoma perronii and other types; Jesús Méndez of the Centro de Apoyo Científico y Tecnológico a la

14

ROLÁN ET AL. : Notes on West African Perrona with the description of a new species

Investigación (CACTI) of the University of Vigo for the SEM photographs; Jesús S. Troncoso for allowing us to use the Photographic apparatus of the Departa-

BIBLIOGRAPHY

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Bernard, P. A., 1984. Seashells ofGabon. Pierre A. Bernard, Libreville, 140 pp.

Bouchet, P. and Rocroi, J.-P., 2005. Classifi- cation and Nomenclátor of Gastropod Fam- ilies. Malacologia, 47(1-2): 1-397.

Boyer, F. and Ryall, P., 2006. Two new Cla- vatulinae species (Caenogastropoda: Turri- dae) from Ghana. Iberus, 24 (2): 33-38

Bruguiere, J.-G., 1792. Encyclopédie Méthodique ou par Ordre de Mtiéres. Histoire Naturelle des Vers. Vol. 1. Part 2. Panckouke, París, pp 345-757.

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Dautzenberg, P., 1912. Mission Gruvel sur la cote occidentale d'Afrique (1909-1910). Mol- lusques marins. Anuales de l'lnstitut Océano- graphique de Monaco, 5: 13-111, 3 pls.

Gmelin, J. F., 1791. Caroli a Linné Systema natu- rae per regna tria naturae, Editio decima tertia, aucta reformata. Leipzig: G. E. Deer. Tome 1, pars 6 (Vermes): 3021-3910.

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Knudsen, R. N., 1952. Marine Prosobranches of Tropical West Africa collected by the "Atlantidae" Expedition 1945-46. Part 1. Videnskabele Meddeleser fra Dansk naturhis- torisk Forening I Kjobenhavn, Bd. 114: 129- 185, pl. 13.

Knudsen, R. N., 1956. Marine Prosobranchs of Tropical West Africa (Stenoglossa). Atlantide Report n° 4. Danish Science Press, Ltd. Co- penhaguen, 1956 pp. 93-105

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Orders et des Genres de ces Animaux Lamarck

and Deterville, París viii + 432 pp.

ment of Ecology of the University of Vigo and Paul-Henri Hattenberger, St. Jean de Blaignac, France for collecting the Congolese specimens.

Lamarck, J. B. P. A. de, 1816. Liste des objets repré- sentés dans les planees de cette livaraison. Tableau encyclopédique et Méthodique des Trois Régnes de la Nature. Mollusques et Polypes Divers. Veuve Agasse, París. 16 pp, pls. 391-488.

Lamarck, J. B. P. A. de, 1822. Histoire Naturelle des Animaux sans Vertébres...Précédée d'une In- troduction Offrant la Détermination des Cha- ractéres Essentiels de Y Animal, sa Distinction du Végétal et des Autres Corps Naturels, Enfin Y - Exposition des Principes Fondamentaux de la Zoologie. Vol. 7. Guiraudet, París. 711 pp.

Maltzan, H. F. von, 1883. Beitráge zurKenntnis der senegambischen Pleurotomiden. Jahr- bücher der Deuschen Malakozoologischen Ges- sellschaf, 10: 115-135, pl. 3.

Maltzan, H. F. von, 1884. Diagnosen neuer se- negambischen Gastropoden. Nachrichtsblatt der Deuschen Malakozoologischen Gessellschaf 16: 65-73.

Marrat, F. P., 1877. A list of West Africa shells, including new Pleurotoma and Columbella. Quarterly Journal of Conchology, 1: 237-244.

Martini, F. H. W. and Chemnitz, J. H., 1788. Neues systematisches Conchylien-Cabinet, vol. 10, 1-376, pls. 137-173.

Nolf, F., 2006. Clavatula nathaliae (Mollusca: Gastrododa: Conoidea: Turridae) a new spe- cies from Gabon: an oíd mystery finally elu- cidated. Neptúnea, 5 (3): 1-14.

Nolf, F. and Verstraeten, J., 2006. Recogni- tion of two new Clavatula species (Mollusca: Gastropoda: Conoidea: Turridae) in a com- plex group from Gabon and North Angola. Neptúnea, 5 (3): 15-29.

Nordsieck, F., 1968. Die europaischen Meeres Gehauseschnecken (Prosobranchia) vom Eismeer bis Kapverden und Mittelmeer. Gustav Fischer, Stuttgart 273 pp.

Petit de la Saussaye, S., 1851. Notice sur un groupe de coquilles classées parmi les Fuse- aux ( Fusus Lam.) avec la description de plusieurs espéces. Journal de Conchyliologie, 2: 73-79, 2 pls.

Powell, A. W. B., 1966. The molluscan families Speightiidae and Turridae an evaluation of the valid taxa, both Recent and fossil, with lists of characteristic species. Bulletin of the Auckland Institute and Museum, 5: 1-184.

Recluz, C., 1851. Description de quelques co- quilles nouvelles. Journal de Conchyliologie, 2 (2):194-216, pls. 5-6.

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Reeve, L. A., 1843-1946. Monograph of the Genus Pleurotoma. Conchologia Iconica, or II- lustrations of the shells of molluscous animáis. Reeve Brothers, London Vol. 1: pls. 1-40, species 1-155, + índex and errata.

Schumacher, C. F., 1817. Essai d'un Nouveau Sy- steme des habitations des vers testacés. Copen- hagen: Schultz. iv + 287 pp, 22 pls.

Strebel, H., 1912. Bemerkungen zu den Clava- tula-G ruppen Perrona und Tomella. Jahrbuch der Hamburgischen Wissenschaftlichen Anstal- ten, 29: 1-24, pl. 1.

Strebel, H., 1914. Mollusca I, Gen. Pusionella. In Michaelsen, W. (Ed.): Beitrage zur Kennt- nis der Meeresfauna Westafrikas, vol. 1, Ham- burg, pp. 87-125, pl. 3.

Sykes, E. R., 1905. Descriptions of new forms of Marginellidae and Pleurotomidae. Proceedings of the Malacological Society, 6: 315-318, lpl.

Tryon, G. W., 1984. Manual of Conchology . Vol. 4 Conidae , Pleurotomidae. Philadelphia, Tr- yon. 151-413, 34 pls.

Tucker, J: K., 2004. Catalog of Recent and fos- sil turrids (Mollusca: Gastropoda). Zootaxa, 682: 1-1295.

ló

Iberus, 26 (1): 17-28, 2008

Pattern of reserve storage of the two mussel species Perna perna and Mytilus galloprovincialis living on Moroccan coasts: annual variation and effect of pollution

Patrones de almacenamiento de reservas en dos especies de mejillón Perna perna y Mytilus galloprovincialis de las costas de Marruecos: variación anual y efecto de la contaminación

Abdellatif MOUKRIM*1, Mohamed ID HALLA*, Abderazak KAAYA*, Abdellah BOUHAIMI*, Soumaya BENOMAR* et Michel MATHIEU**

Recibido el 23-XI-2005. Aceptado el 30-X-2007

ABSTRACT

The pattern of reserve storage and ¡ts ¡mportance ¡n the reproductive cycle of the two mus- sel species living in Moroccan coasts, Perna perna and Mytilus galloprovincialis, were studied comparatively, during two annual cycles. Study was conducted at a polluted and an unpolluted site in Agadir bay. Stereological analysis shows that P. perna presents only one type of storage cells (vesicular cells) storing glycogen. In M. galloprovincialis, two types of storage cells are present: vesicular cells and adipogranular cells (containing glycogen, lipids and proteins). In both species, seasonal variations of reserve tissue vol- ume are conversely proportional to those of the germinal tissues. Reserve tissue appeared in spring (May) and increased in summer. It decreased quickly from August onwards, and disappeared between January and April. In M. galloprovincialis, adipogranular cells dis- appeared before vesicular cells and reappeared first. In the polluted site, seasonal varia- tion of reserve and germinal tissues is comparable to that in unpolluted site but the máxi- mum valué of reserve tissue percentage is less ¡mportant. Moreover, during the year, this tissue did not disappear. Biochemical analysis shows that mean valúes of glycogen and proteins quantities are significantly higher in P. perna than in M. galloprovincialis. How- ever, total lipids quantity mean is higher in M. galloprovincialis. Seasonal variations of the three biochemical parameters present a similar profile in the two species. Compared to unpolluted site animáis, in polluted one, molluscs possess low glycogen and high lipids lev- éis. Seasonal variations of these parameters show a perturbed profile.

RESUMEN

Se ha estudiado y comparado el patrón de almacenamiento de reservas y su importancia en el ciclo reproductor en dos especies de mejillón de las costas de Marruecos, Perna perna y Mytilus galloprovincialis, durante dos ciclos anuales. Este estudio se llevó a cabo en un sitio contaminado y otro no contaminado de la bahía de Agadir. El análisis estere- ológico demostró que P. perna presenta un solo tipo de células de reserva (células vesicu- lares) almacenando glucógeno. En M. galloprovincialis, hay dos tipos de células de

* Laboratory Aquatic Ecosystems: Marine and Continental Field, Biology Department, Sciences Faculty, Ibn Zohr University, BP 8106, 80000, Agadir, Morocco.

** Laboratory Marine Biology and Biotechnology, I. B. B. A., Caen University, France.

1 Corresponding author.

17

Iberus , 26 (1), 2008

reserva: células vesiculares y células adipogranulares (conteniendo glucógeno, lípidos y proteínas). En ambas especies, las variaciones estacionales del volumen de tejido de reserva son inversamente proporcionales a las del tejido germinal. El tejido de reservas apareció en la primavera (mayo) y se incrementó en verano. A partir de agosto, dismin- uyó rápidamente y desapareció entre enero y abril. En M. galloprovincialis, las células adipogranulares desaparecieron antes que las células vesiculares y son las primeras en aparecer en el siguiente ciclo. En el sitio contaminado, la variación estacional de tejidos de reserva y germinales es similar a la del sitio no contaminado, salvo que el porcentaje máximo de tejido de reserva es menor. Además, este tejido no desapareció a lo largo del año. Los análisis bioquímicos muestran que las cantidades promedias de glucógeno y de proteínas son significativamente más altas en P. perno que en M. galloprovincialis. Sin embargo, el promedio de lipidos totales fue mayor en M. galloprovincialis. Las varia- ciones estacionales de los tres parámetros presentan un perfil similar en las dos especies. Comparados con los del sitio no contaminado, los animales del sitio contaminado poseen niveles bajos en glucógeno y altos en lípidos. Las variaciones estacionales de estos parámetros muestran un perfil perturbado.

KEY WORDS: Agadir, Morocco, mussels, Mytilus galloprovincialis, Perna perna, pollution effects, reproductive cycle, reserves strategy.

PALABRAS CLAVE: Agadir, Marruecos, mejillones, Mytilus galloprovincialis, Perna perna , efectos de la conta- minación, ciclo reproductor, estrategias de reserva.

INTRODUCTION

Two sympatric mussel species are found along the Moroccan coast: the African mussel Perna perna and the Mediterranean mussel Mytilus gallo- provincialis. The first species is located in the north of its geographical distribu- tion; the second one in its Southern limit. In Agadir bay, these local popula- tions of mussels have important com- mercial valúes (Id Halla, 1997) and environmental interest (Najimi, Bouhaimi, Daubéze, Zekhnini, Pel- LERIN, NARBONNE, AND MOUKRIM, 1997; Kaaya, Najimi, Ribera, Narbonne, and Moukrim, 1999; Moukrim, Kaaya, Najimi, Roméo, Gnassia-Barelli, and Narbonne, 2000) as sentinel species.

The few studies carried out on mussel biology in this area, concern only some aspects of the reproduction cycle (Shafee, 1989; Id Halla, Bouhaimi, Zekhnini, Narbonne, Mathieu, and Moukrim, 1997). They showed that P. perna and M. galloprovin- cialis present synchronous reproductive cycles, and breed throughout the year with a principal spawning period in spring. The only differences observed

by Id Halla et al. (1997), regard the duration of the principal spawning period (more important for P. perna ) and the genital activity rhythm in summer (reduced in this species).

In view of the importance of reserves in the reproductive cycle (Bayne, Bubel, Gabbott, Livingstone, Lowe and Moore, 1982; Lowe, Moore and Bayne, 1982; Pipe, 1987) and of the particularities of reserve strategy in Mytilidae (strategy essentially based on the glycogen, presence of specific storage cells and existence of a direct relationship between reserve metabo- lism and reproductive cycle), it was interesting to conduct a comparative study of P. perna and M. galloprovincialis in order to describe the reserves strat- egy for these two species living in the same environmental conditions. The two molluscs present an important dif- ference regarding the cells involved in the reserve storage. As indicated by Lunetta (1969) P. perna presents only one type of storage cells (vesicular cells or glycogen cells), storing especially the glycogen ; however, in M. galloprovin-

18

Moukrim ET AL.: Reserves strategy of mussels in Moroccan coasts

cialis (Herlin-Houtteville, 1974; Dan- ton, Kiymoto, Komaru, Wada, Awaji and Mathieu, 1996), two types of storage cells are present, vesicular cells (storing glycogen) and adipogranular cells (containing glycogen, lipids and proteins).

Furthermore, beyond the determina- tion of pattern of reserve storage and its importance in the reproductive cycle of the two mussels living in Moroccan coasts, this work studies the impact of pollution on this pattern. Therefore, a comparative study of two sites (unpol- luted and polluted) was conducted.

MATERIAL AND METHODS

Sampling

This study was conducted during two annual reproductive cycles (October 1994 to August 1996). Two types of sites, representative of the Agadir marine bay were considered: i) a reference site (unpolluted). Cap Ghir, located 50 km north of Agadir City and far from any human activity, and ii) a polluted site (Anza) located 5 km north of Agadir and receiving the industrial and domestic untreated waste waters of Anza zone. Many studies, conducted during the same period of the present study, showed that this site is contami- nated by heavy metáis and PAHs either accumulated by mussels or in sediment (Id Halla, 1997; Najimi, 1997; Moukrim, Kaaya, Najimi, Roméo, Gnassia-Barelli and Narbonne 2000; Kaaya, 2002), with some perturbations in the physical and Chemical parameters of seawater (Id Halla, 1997).

During this study, for each month, ninety individuáis of 35 mm for each species are collected at random in each of the two sites. 30 individuáis/ species/sites were subject to stereologi- cal analysis and 60 individuáis/ species/sites were dedicated to the bio- chemical analysis.

Stereological analysis

In order to follow the seasonal vari- ation of the glycogen according the

reproduction cycle in Mytilus gallo- provincialis and Perna perna, an histo- chemical study (stereological analysis) was conducted in the mantle. Thirty adult mussels were collected and directly fixed in Gendre liquid for 3 days. Animáis were then removed from shells and a central portion of mantle tissue was correctly excised and embed- ded in paraffin. Sections of 6 pm were cut and stained by the periodic acid of Schiff (PAS). Stereological analysis was applied according the method of Weibel, Kistler, and Scherle (1966) which quantified the volume occupied by the reserve and germinal tissues. The cell types were determined accord- ing the definition of Lubet (1959): i) adipogranular cells (20-25 pm for length, 4.5-5 pm for length of nucleus, green coloration, contain lipids, pro- teins and glycogen), and ii) vesicular cells (50-80 pm for length, 3-5 pm for length of nucleus, pink coloration, contain only glycogen)

Biochemical analysis

Biochemical analysis (glycogen, lipids and proteins) was carried out on mussel mantle which in Mytilidae, con- stitutes an important organ in storage of reserves. Monthly, sixty adults were ran- domly sampled, quickly transferred to the laboratory in isotherm conditions and frozen at -30°C. Glycogen, total lipids and proteins were respectively measured according the methods of Duchateau and Florkin (1959), Folch, Lees and Sloane-Stanley (1957) and Lowry (1951). Rates of these compounds were expressed as mg/g fresh weight (mg/ g FW).

Statistical analysis

Stereological analysis was expressed as a percentage of the total volume of mantle tissue ; biochemical results as means ± standard deviations. The statis- tical significance of difference between samples was evaluated by the "t" test using the Statistica software (Release 4.5 A StatSoft Inc. Ed. 1993). A "P" valué of less than 0.05 was considered as sta- tistically significant.

19

Iberus , 26 (1), 2008

Figure 1. Cells implicated in the reserve storage in Perna perna (A) (only one type of cells: ve: vesicular cells) and Mytilus galloprovincialis (B) (two types of cells, ve: vesicular cells; adge: adi- pogranular cells). Scale bars 10 pm.

Figura 1. Células implicadas en la acumulación de reservas en Perna perna (A) (solo un tipo de células: ve: células vesiculares) y Mytilus galloprovincialis (B) (dos tipos de células, ve: células vesiculares; adge: células adipogranulares). Escalas 10 pm.

RESULTS

Stereological analysis

Figure 1A shows that the mantle of Perna perna presents only one type of storage cells: vesicular cells (VC). In Mytilus galloprovincialis (Fig. IB), two types of storage cells are presentí adi- pogranular cells (ADGC) and vesicular cells (VC).

For P. perna, the respective volumes of germinal and reserve tissues are con- versely proportional (Fig. 2A). The sea- sonal profile is similar during the two studied annual eyeles. The volume of germinal tissue increases from October to February, when the máximum is reached (respectively 72% and 77% in the first and second year). From March onwards, the germinal tissue volume decreases to reach the minimum in August (respectively 8% and 6% in the first and second year). The reserve tissues appeared in spring (May) and increased until reaching maximal valúes in summer (August). They decreased quickly and disappeared between January and April. In the polluted site (Fig. 3A), the seasonal variation of reserve and germinal tissues is similar to that in the reference site but the máximum valué of reserve tissues per-

centage is lower (57% and 62% respec- tively in the first and second year). Moreover, during the year, this tissue did not disappear. The minimum valué recorded was 7-10% in February.

For Mytilus galloprovincialis (Fig. 2B), the volume of germinal tissue increases in autumn and in the beginning of winter to reach a máximum in February (75%). Thereafter, we observe a reduc- tion of the surface occupied by this tissue until October where the minimum (12%) is reached. During the second eyele a similar evolution is recorded. Otherwise, as with P. perna, the volume of germinal tissue is inversely proportional to reserve tissue. Nevertheless, in this case, the máximum is reached in October (64%), whereas the disappearance takes place from January to March for the two studied yearly eyeles. In the polluted site (Fig. 3B), the reserve tissue presents a seasonal evolu- tion similar to the reference site. Besides, this tissue never disappears as in P. perna. The occupied minimal volume is 5% reached in February.

Moreover, for M. galloprovincialis, in the reference site, the adipogranular cells disappeared before the vesicular cells and then reappeared first. In the polluted site the two cellular categories persist

20

Moukrim ET AL. : Reserves strategy of mussels in Moroccan coasts

A

Reserve tissue ^ Germinal tissue O Others

B

100%

90%

OND JFMAM J JASOND JFMAM J JA

ADGC

VC

Germinal tissue

I | Others

Figure 2. Seasonal variation of germinal and reserve tissues in Perna perna (A) and Mytilus gallo- provincialis (B) in the unpolluted site. (VC: vesicular cells storing glycogen; ADGC: adipogranular cells, containing glycogen, lipids and proteins).

Figura 2. Variación estacional de los tejidos germinal y de reservas en Perna perna (A) y Mytilus gallo- provincialis (B) en el sitio no contaminado. (VC: células vesiculares almacenando glucógeno; ADGC: células adipogranulares, conteniendo glucógeno, lípidos y proteínas ).

during all the year. However, an oscilla- tion can be observed in the volumes occupied by the two categories of cells.

Biochemical analysis

Glycogen: The mean amount of glycogen is significantly (F= 11.19 and P= 0.027) higher in Perna perna than in Mytilus galloprovincialis (respectively 59.6 ± 7.36 and 48.7 ± 4.78 mg/g FW). For the two species, the seasonal varia- tions are significant (F= 4.95 ; P= 10"6 for

Perna perna and F= 2.65 ; P= 4.7xl0'6 for Mytilus galloprovincialis) and exhibit a similar profile (Fig. 4A). The glycogen increases in spring (from April), reaches a maximal valué in August (219.4 and 191.9 mg/g FW in Perna perna and Mytilus galloprovincialis respectively), then decreases during autumn and winter. The minimal valúes are noted in February (0.39 and 0.34 mg/g FW in Perna perna and Mytilus galloprovincialis respectively).

21

Iberus, 26 (1), 2008

ioo%-

90% - 80% - 70% ' 60% - 50% - 40% ' 30% ' 20% ' 10%' o%-

i

¡i

i I

li

I

l

i

i ¡ I

p

II

lli

Wm

i i

11.

li

,1

H

1*

"

L

i

■I

i»

1

OND JFMAM J JA SOND JFMAM J JA

Reserve tissue ^ Germinal tissue Q Others

100%

90%

80%

70%

60%

50%

40%

30%

20%

10%

0%

B

Figure 3. Seasonal variation of germinal and reserve tissues in Perna perna (A) and Mytilus gallo- provincialis (B) in the polluted site. (VC: vesicular cells storing glycogen; ADGC: adipogranular cells, containing glycogen, lipids and proteins).

Figura 3. Variación estacional de los tejidos germinal y de reservas en Perna perna (A) y Mytilus gallo- provincialis (B) en el sitio contaminado. (VC: células vesiculares almacenando glucógeno; ADG: células adip ogranulares, conteniendo glucógeno, lípidos y proteínas).

ONDJFMAMJ JASONDJFMAMJ JA ¡H ADGC H VC ^ Germinal tissue Q Others

In the polluted site (Fig. 4B), the dif- ference between the mean amount of glycogen in the two species (39.75 and 23.44 mg/g FW in P. perna and Mytilus galloprovincialis respectively) is not sig- nificant (F= 6.257 and P= 0.130). Other- wise, their seasonal variation are signifi- cantly different (F= 4.03 and P= 10'6 in P. perna and F= 9.78 and P= 10~7 in M. galloprovincialis). The seasonal profile is completely different for the two mol- luscs: For P. perna , it presents three

peaks, the first in June (96.05 mg/ g FW), the second in November (118.87 mg/g FW) and the third in May of second year (159.02 mg/g FW). For M. galloprovin- cialis, only two peaks are recovered 65.03 and 153.64 mg/g FW respectively in May and November of the first year.

The comparison of valúes for refer- ence and polluted site animáis shows a significant difference. The valúes in the polluted site are less important (39.8 ± 13.36 instead of 59.6 ± 7.36 mg/g FW in

22

Moukrim ET AL Reserves strategy of mussels in Moroccan coasts

P perna ▲ M. galloprovincialis

Month

Figure 4. Seasonal variation of glycogen in the mantle of Perna perna and Mytilus galloprovincialis in the reference site (A) and the polluted site (B)

Figura 4. Variación estacional del glucógeno el el manto de Perna perna y Mytilus galloprovincialis en el sitio de referencia (A) y en el sitio contaminado (B)

the reference site, for Perna perna). More- over, the seasonal profile of glycogen contení (Fig. 4B) presents some pertur- bations compared to the reference site.

Lipids : A significant difference was noted between the mean amounts of total lipids in the two mussels species (92.86 and 125.04 mg/g FW in P. perna and Mytilus galloprovincialis respectively). However, the difference of their seasonal variation are significant with F= 4.42 and P= 10'6 in P. perna and F= 3.6 and P= 4.5xl0'5 in M. galloprovincialis. In the first year, the seasonal profile (Fig. 5A) is similar for the two molluscs. The lipid contení increased in autumn, with a maximal valué in December (respectively 354.3 and 316.9 mg/ g FW in Perna perna and Mytilus gal- loprovincialis), and decreased in winter and spring. However, in the second year, a slight increase was noted in summer (June - July) only in P. perna.

In the polluted site, the two species present a significant difference between total lipids mean valúes (respectively 231.4 ± 21.47 and 135.5 ± 16.93 mg/g FW in Perna perna and Mytilus gallo- provincialis). Besides, the difference in their seasonal variation (Fig. 5B) is sig- nificant with F= 2.59 and P= 0.002 in P. perna and F= 3.60 and P= 4.5xl0"4 in M. galloprovincialis.

Ótherwise, the valúes are generally higher for the polluted site than the ref- erence site for the two species. More- over, compared to the unpolluted site, the seasonal variation (Fig. 5B) shows a perturbed profile with several peaks during the annual cycle and a máximum valúes is reached rather in August (777.03 mg/ g FW in P. perna and 659.95 mg/g FW in M. galloprovincialis).

Proteins : The mean contení of protein is significantly higher in Perna perna (28.9

23

Iberus, 26 (1), 2008

P. perna a M. galloprovincialis

Month

Figure 5. Seasonal variation of lipids in the mantle of Perna perna and Mytilus galloprovincialis in the reference site (A) and the polluted site (B).

Figura 5. Variación estacional de los lípidos en el manto de Perna perna y Mytilus galloprovincialis en el sitio de referencia (A) y en el sitio contaminado (B).

± 3.51 mg/g FW) compared to Mytilus galloprovincialis (20.2 ± 3.17 mg/g FW). However, the seasonal profile (Fig. 6A) is similar for the two species. The maximal valúes were generally recorded in summer and autumn in the first year and in winter and beginning spring in the second year, whereas the minimal valúes were reached at the end of autumn and the beginning of winter.

In the polluted site (Fig. 6B), the mean amount of protein is higher in P. perna (30.11 ± 7.742 mg/g FW) than in M. galloprovincialis (19.74 mg/g FW). However, the mean valúes and the sea- sonal profile do not show any signifi- cant difference compared with those observed from the reference site (F= 1.08 and P= 0.30 for Perna perna ; F= 0.31 and P= 0.57 for Mytilus galloprovincialis ). For the two species, the máximum valúes were recorded in summer and autumn.

DISCUSSION

The comparative study of the reserve pattern of the two mussels species living in the Moroccan coasts, Perna perna and Mytilus galloprovincialis, sampled in the same site (Cap Ghir, Agadir bay), shows that, in spite of the difference in their reserve tissues (only one cell type, vesicular cells, in Perna perna ; two cell types, adipogranular cells and vesicular cells, in Mytilus gallo- provincialis), the two molluscs have a similar fluctuation.

This strategy presents cycles (of re- serve compounds and cells involved in the storage) which, compared to the cy- cle of reproduction (determined in these same animáis by Id Halla et al., 1997) are inversely proportional to it. The ac- cumulation of reserves in these cells is related to the period of reduced sexual

24

Moukrim ET AL. : Reserves strategy of mussels in Moroccan coasts

P. perna a M. galloprovincialis

Figure 6. Seasonal variation of proteins in the mantle of Perna perna and Mytilus galloprovincialis in the reference site (A) and the polluted site (B).

Figura 6. Variación estacional de las proteínas el manto de Perna perna y Mytilus galloprovincialis en el sitio de referencia (A) y en el sitio contaminado (B).

activity (in summer). The low levels of reserve are obtained in autumn and par- ticularly in winter (gametogenesis and spawning periods). Similar results have been reported in Perna perna from Brazilian coasts (Lunetta, 1969) and in Mytilus galloprovincialis from the French coasts (Herlin-Houtteville, 1974; Danton, Kiymoto, Komaru, Wada, Awaji and Mathieu, 1996). Also, in the Ria de Vigo (Spain), the profile of the variations of the gonadic Índex and so- matic Índex in cultured mussels show clearly their inverse and gradual fluctu- ations (Cáceres-Martínez and Figueras, 1998). This association be- tween gonad and storage tissue cycles in mussels is well known. Decline of the ADG cells occurs during gametogenesis by a lysosomal autophagic mechanism (Bayne et al., 1982; Lowe, Moore and Bayne; 1982; Pipe, 1987). The energy

used in gonad restoration following spawning during spring and summer probably derived directly from feeding since ADG cells disappeared from the mantle in early spring (Villalba, 1995).

Furthermore, the reserve accumula- tion in the two mollusc species is related to the proliferation of the phytoplanc- tonic biomass linked to upwelling cur- rents which take place, between Febru- ary and August, in the Agadir bay and more precisely in Cap Ghir (Belveze, 1984 ; Agoumi and Orbi, 1992). Cáceres-Martínez and Figueras (1998) reported that this increase in food availability for mussels in the area favours the accumulation of reserves during this period. These results also confirm the cióse dependence, described by Mathieu (1987), between the reserve storage and environmental conditions in marine ecosystems. As suggested by

25

Iberus, 26 (1), 2008

this author, the disappearance of reserve tissue in mussels seems to be under endocrine control via cerebroid ganglia which provoke disappearance of adi- pogranular cells and vesicular cells in the mantle after liberation of their reserves which are indispensable for gametogenesis and spawning process. The synchronic character of this disap- pearance, in Perna yerna and Mytilus gal- loyrovincialis, could be explained by the existence of the same mechanism for the control of reserves in both species.

The comparison of the reserve com- pounds in the two molluscs shows that the glycogen, total lipids and proteins contents are higher in Perna yerna (in spite of the presence of only one type of reserve storage cells, vesicular cells) compared to Mytilus galloyrovincialis. These results could explain the differ- ences observed by Id Halla et al. (1997) between the reproductive cycles of these bivalves. According to these authors, in Perna yerna, compared to Mytilus galloyrovincialis, the main- spawning period in spring is longer and the sexual activity in summer is reduced. Otherwise, the important reserve levels in this species could be attributed to the spatial distribution of each species: Perna yerna lives essen- tially at the infra-littoral level and is more immersed than Mytilus galloyrovin- cialis (Id Halla et al., 1997) and, conse- quently, has access to more nutrients, thus allowing the synthesis and storage of more reserves. Seed (1976) showed that the gonadal development was faster in mussels from the low intertidal zone, than in those from the upper zone and related these results to food avail- ability. Other studies associated local variations in gonadal cycle with envi- ronmental conditions (Ferrán, 1991; Villalba, 1995). According to Cáceres- Martínez and Figueras (1998), there is no influence of locality and depth in the gonadal development of cultured mussels.

The seasonal profile of the biochemi- cal reserves studied shows that the first peak of glycogen and lipids, recorded in summer, is related to the occurrence of

upwelling currents which provide food availability, ensuring an abundant planktonic food supply for mussels. According to Cáceres-Martínez and Figueras (1998), massive spawns occur in spring coinciding with an increase in temperature and chlorophyll-a concen- traron in the area providing favorable conditions for larval growth. In winter, the second peak of lipids coincides with the maturity period of gametes. This peak takes place just after the disap- pearance of the glycogen peak. It is probably a result of the glycogen trans- formaron. The metabolic conversión of glycogen to lipids has been reported by Zaba and Davies (1980), using 14C- glucose. According to Gosling (1992), the mantle is considered as the organ of many and extensive metabolic transfor- mations during the sexual cycle. The reserves, particularly the glycogen, accumulated during summer, are used in autumn and winter for the gametoge- nesis. Similar results were reported by Shafee (1989) in Perna yicta of Temara (North of Morocco).

In the polluted site (Anza), many perturbations in the metabolism of reserves were noted comparatively to the reference site (Cap Ghir). The reserve tissues, which disappeared in winter and at the beginning of spring, in mussels of Cap Ghir, persist throughout the sexual cycle in Anza mussels. This could probably be a result of the pollu- tion effect on the cerebroid ganglions neurosecretions which are, according to Lubet, Herlin, Mathieu, and Collin (1976) and Mathieu (1987) involved in the control of reserve cells.

The analysis of the seasonal profile of the reserve levels in mussels sampled in the polluted site shows some pertur- bations as compared to the reference site. For example, the glycogen content is low in summer (August), in spite of the availability of phytoplanctonic biomass in this period. This is probably linked to the stress caused by pollution of industrial and domestic waste waters discharged directly in this site, without any treatment. This fact was indicated by Deslous-Paoli, Wolowicz, and

26

Moukrim ET AL.: Reserves strategy of mussels in Moroccan coasts

Boromthanarat (1991) who reported that, in Mytilus edulis, reserves could be used both in reproductive process and to overeóme the hard environmental conditions. According to Thompson (1972) the reserves are used in order to reach the basal level of energy necessary for stressed animáis.

Contrary to the glycogen, the total lipids are more important in Perna yerna and Mytilus galloprovincialis living in Anza (polluted site). This could be explained by an eventual direct assimi- lation of lipids from the organic matter of waste waters and/or a change of the reserve storage process. According to Gosling (1992) the lipid storage process in molluscs is considerably linked to the environmental conditions, particularly to the presence of pollutants.

As a general conclusión, in the two species of mussel P. yerna (with only vesicular cells) and M. galloprovincialis (with adipogranular cells and vesicular cells), the respective germinal and reserve tissues clearly show their inverse and gradual profile. Their sea- sonal fluctuations are similar in the two molluscs. In the polluted site, many per- turbations of the reserve metabolism were noted comparatively to the refer- ence site. Then, contrary to animáis of this latter site, which presented a glyco-

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Belveze, H., 1984. Biologie et dynamique des pop- ulations de la sardine (Sardina pilchardus Wal- baum) peuplant les cotes atlantiques du Maroc. Thése de Doctorat d'Etat, Université de Bre- tagne Occidentale, Brest: 229 pp. Cáceres-Martínez, J. and Figueras, A., 1998. Long-term survey on wild and cultured mus- sels ( Mytilus galloprovincialis Lmk.) repro- ductive eyeles in the Ria de Vigo (NW. Spain). Aquaculture, 162: 141-156.

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The results obtained in this work constitute a contribution to the knowl- edge of the reserve strategy in the two species living along Moroccan coasts, the African mussel Perna yerna and the Mediterranean mussel Mytilus gallo- yrovincialis. So, several faets are reported: i) the type, the seasonal variation and the eyele of the reserve strategy in the two molluscs, ii) cells involved in the storage,

iii) the relationship between the reserve strategy and the reproduction eyele, and

iv) the response of this strategy to the environmental conditions. Nevertheless, it would be interesting to identify the mechanism and the control process of the reserve strategy in these molluscs.

ACKNOWLEDGMENTS

We are grateful to Miss Joanne Preston (Southampton University, UK) and Mrs Barbara Picot (Angers Univer- sity, France) for their Language correc- tions. We thank the IFS (Sweden), AUPELF (Cañada), Ministére des Affaires Etrangéres (France) and Min- istére de l'Enseignement Supérieur et de la Recherche Scientifique (Morocco), for their financial assistance.

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Najimi, S., Bouhaimi, A., Daubéze, M., Zekhnini, A., Pellerin, ]., Narbonne, J. F. and Moukrim, A., 1997. Use of acetyl- cholinesterase in Perna perna and Mytilus gal- loprovincialis as a biomarker of pollution in Agadir marine bay (South of Morocco). Bul- letin ofEnvironmental Contamination and Tox- icology, 58: 901-908.

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Shafee, M. S., 1989. Reproduction of Perna perna (Mollusca: Bivalvia) from the atlantic coast of Morocco. Marine Ecology Progress Se- ries, 53: 235-245.

Thomspon, R. ]., 1972. Feeding and metabolism in the mussel Mytilus edulis L. Ph.D Thesis, University of Leicester: 186 pp.

Villalba, A., 1995. Gametogenic cycle of cul- tured mussel, Mytilus galloprovincialis, in the bays of Galicia (NW Spain). Aquaculture, 130: 269-277.

Weibel, E. R., Kistler, G. S. and Scherle, W. F., 1966. Practical stereological methods for morphometric cytology. Journal ofCell Biol- ogy, 30: 23-38.

Zaba, B. N. and Davies, J. ]., 1980. Glucose metabolism in an in-vitro preparation of the mantle tissue from Mytilus edulis L. Marine Biology Eetters, 1: 235-243.

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Iberus, 26 (1): 29-42, 2008

Reproduction of the cockle Cerastoderma edule (Linné, 1758) in the estuary of Oued Souss (southwestern Morocco)

Reproducción del berberecho Cerastoderma edule (Linné, 1758) en el estuario del Oued Souss (suroeste de Marruecos)

Hafida BERGAYOU**, Abdellatif MOUKRIM*1, Michel MATHIEU** and Jean-Pierre GIMAZANE**

Recibido el 14-11-2006. Aceptado el 3 l-X-2007

ABSTRACT

Field and laboratory investigations were carried out from 2001 to 2003 on a population of Cerastoderma edule living ¡n the estuary of Oued Souss, ¡n order to determine the impact of domestic wastewater discharges on the biology of this species. During waste- water discharges, several episodes of partial spawning occurred from November to March, followed by another in April-May. The main spawning occurred nevertheless in August. The gonadic Índex was always higher than 1, so that the period of sexual rest was short. The period of recruitment (from June to October) was mainly correlated with spawning peaks. The renewal of the population was ensured by the recruitment of June- July, whereas young cockles recruited from August to October only represented 9.2% of the population at the end of autumn. Most 1-year-old cockles disappeared during the sum- mer of the second year following their recruitment. After wastewater pollution stopped, an important recruitment of young cockles occurred. The spatial distribution of this species progressed upstream and the biomass of cockles had strongly increased. Because of its reproduction which takes place throughout the year, C. edule , as an opportunistic species, succeeded in colonizing this site.

RESUMEN

Se realizaron, entre 2001 y 2003, estudios de campo y de laboratorio sobre una pobla- ción de Cerastoderma edule del estuario del Oued Souss, con el objetivo de determinar el impacto de los vertidos de aguas residuales sobre la biología de esta especie. Coinci- diendo con los vertidos, se produjeron varios episodios de puesta parcial entre Noviem- bre y Marzo, seguidos de otro en Abril-Mayo. La puesta principal, sin embargo, se pro- dujo en Agosto. El índice gonádico fue siempre superior a 1 , indicando que el periodo de reposo sexual fue corto. El periodo de reclutamiento (de Junio a Octubre) estuvo esencial- mente relacionado con picos de puesta. La reposición de la población fue asegurada por el reclutamiento de Junio-Julio, mientras berberechos jóvenes reclutados entre Agosto y Noviembre representaban tan solo el 9,2% de la población a finales de otoño. La mayor parte de los berberechos con un año de edad desaparecieron durante el verano del segundo año después de su reclutamiento. Al finalizar los vertidos se produjo un impor- tante reclutamiento de berberechos jóvenes. La especie se extendió río arriba y la bio-

* Laboratory Aquatic Ecosystems : Marine and Continental Field, Biology Department, Sciences Faculty, Ibn Zohr University, BP 8106, 80000, Agadir, Morocco.

** Laboratory of Marine Biology and Biotechnology, University of Caen, F- 14000, Caen, France.

1 Corresponding author

29

Iberus , 26 (1), 2008

masa de berberechos aumento fuertemente. Por su reproducción que se extiende sobre todo el año, C. edule, como especie oportunista, fue exitosa en la colonización de este lugar.

KEY WORDS: Cerastoderma edule, estuary, Oued Souss river, pollütion, recruitment, reproductive cycle, waste- water discharges.

PALABRAS CLAVE: Cerastoderma edule, estuario, Oued Souss, contaminación, reclutamiento, ciclo reproductor,

INTRODUCTION

In marine environment, many biotic and abiotic factors may influence the life cycle of bivalves. If temperature, salin- ity, food supply, and tidal exposure are the most important causes known to modulate development in mytilids (Seed, 1975), other elements, such as intraspecific competition or environ- mental contaminants, can result in great variations in growth rate of bivalves (Seed and Suchanek, 1992). These factors also have an effect on the repro- duction, settlement, recruitment, and production of these molluscs so that their variations directly affect the devel- opment of beds for each species of bivalve (Widdows and Donkin, 1992).

Contrary to numerous ecological reports on the effects of contaminants on different marine bivalves, the recovery of mollusc populations after the disap- pearance of pollütion has been less investigated.

The implantation of a wastewater pu- rification plant since November 2002 along the estuary of Oued Souss, at 4 km from the mouth of the estuary, had re- sulted in the fact that the fresh water still running in the river and the decanted wastewater were no longer discharged in the estuary but diverted to another Coastal site: M'Zar, located at 3 km south. For this reason, the estuary, upstream to the purification plant, was only swept by sea tide at the present time.

As there existed a population of Cerastoderma edule living in the estuary of the Oued Souss river, it was interest- ing to determine the physiological State of these cockles during the pollütion period by wastewater and the changes which have occurred after this contami-

nation stopped. In view of these objec- tives, the following two questions aróse: Had the discharge of wastewater before November 2002 caused repercussions on the reproductive cycle of C. edule and on the dynamics of this population? What consequences did the presence of sea water in the estuary after November 2002 have on the spatial distribution and biomass of C. edule? To answer the first question, monthly investigations from January 2001 to December 2002 were carried out in the habitat of C. edule i) to follow the different stages of sexual maturity in males and females, and ii) to specify the development of the different generations and cohorts of cockles. To tackle the second question, two surveys in 2002 and 2003 during summer months were performed in the estuary of Oued Souss river.

This study complements other reports made by our research team in the same ecosystem (Mouneyrac, Pel- LERIN, MOUKRIM, AlT ALLA, DUROU AND

Viault, 2005; Ait Allá, Mouneyrac, Durou, Moukrim and Pellerin, 2005; Ait Allá, Gillet, Deutsch, Moukrim and Bergayou, 2005; Bergayou and Moukrim, 2003 and Gillet, Gorman, Tallec, Moukrim, Mouloud, Anajjar, Ait Allá, Bergayou and Kaaya, 2003).

MATERIALS AND METHODS

The estuary of Oued Souss is located on the Atlantic coast, in southwestern Morocco and is subjected to an arid climate. The mouth is swept by an intense marine hydrodynamism, responsible of the presence of great

30

Bergayou ET AL.: Reproduction of Cerastoderma edule in Southwestern Morocco

Figure 1 . Location of sampling sites along the estuary of Oued Souss in the Bay of Agadir, south- western Morocco.

Figura 1. Situación de las localidades de maestreo a lo largo del estuario del Oued Souss, en la bahía de Agadir, suroeste de Marruecos.

sandbanks in the estuary, with currents linked to high or low tides, and with high salinity (from 31.2 to 34.2 %o).

Reproductive cycle

The study of reproductive cycle and population dynamics for C. edule were carried out at station 2 (30° 21.97'N north, 9o 35.98'W west), (Fig. 1). Selected because of its high biomass of the cockle population, this station was character- ized by fine silty sand 2-5% of organic matter in the substratum and 340-440 mg/1 of suspended matter in the water.

Two methods for studying the repro- ductive cycle of C. edule were used. The first was a classical histological study of gonads and was performed from January 2001 to March 2002. The second was a complementary study of condi- tion Índex and microscopic examination of gonad smears (Guillou, Bachelet, and Glémarec, 1991) and was per- formed from August 2001 to August 2002. For the first and second study.

respectively, 30 and 100 cockles (length, 20 to 30 mm) were collected by hand at low tide, at monthly intervals (respec- tively, a total of about 450 and 1300 accumulated cockles was examined).

For the first study (histological study of gonads), the shells of C. edule were opened and soft masses were prefixed in the Gendre's fixative for 24 h. In the laboratory, the shell of each bivalve was removed and small pieces of soft masses were post-fixed in a new solution of Gendre's fixative for 48 h before being dehydrated through a graded series of ethanol and butanol, and finally embed- ded in cytoparaffin (56°-58°C). Serial sections (thickness, 5 pm) were made before being stained with Gabe's trichrome, hemalun-eosin, or Mann- Dominici's method (Gabe, 1968). The maturity of gonads was determined using the scale proposed by Lubet (1959) for Mytilus edulis (Table I).

The gonadic Índex (Seed, 1975) indi- cates the State of gonad maturity for

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Iberus, 26 (1), 2008

Table I. Terminology used by LUBET (1959) and LUCAS (1965) to study morphologically and his- tologically the gonadic developmental stages in bivalves.

Tabla I. Terminología empleada por Lubet (1959) y Lucas (1965) para el estudio morfológico y his- tológico de estadios de desarrollo gonadal en bivalvos.

Lubft's scale (1959)	Lucas's scale (1965)
Staqe 0: sexual rest. Staae 1: earlv qametoaenesis with numerous qoniae. Staqe III D: spent, completelv emptv lumina.	Staqe A: sex undetectable. Ihis stage can correspond to sexual rest, previtellogenesis, or gamete resorption.
Staqe II: activelv developinq qonads but mature qametes were not observed.	Staqe B: sex detectable with difficully to the naked eye.
Staqe IIIA: near ripe follides with mature qametes. Staqe IIIB: spawninq, follicles distended.	Staqe C: identifiable gonad. Ihe foot is salmon-stained in males and pearly white in females. Gonad maturation and spawning occurred during this stage.
Staqe IIIC: partial spawninq, partiallv emptv lumina.	Staqe D: gonadic reconstitution with co-existence of empty follicles and of tubules showing numerous goniae.
each population and is evaluated from histological slides. It was determined by giving a number to each of Lubet's gametogenic stages: stage 0 (number 1), stages I and II (2), stage IIIA (3), stages IIIB and IIIC (2), and stage IIID (1). For each sample of cockles, the number of gonads showing a gametogenic stage is multiplied by the corresponding number; the figures obtained were then added and the sum was then divided by the total number of cockles studied. This gonad Índex varied from 1 (all gonads were spent, with completely empty lumina) to 3 (all gonads were ripe). The stereological analysis was made on the whole bivalves used for the histo- logical examinations of gonads. For each C. edule, three histological slides were randomly chosen through the antero- posterior axis. The different cell cate- gories present in gonadic follicles were counted on five ocular fields (magnifica- tion: x 100 for females, and x 400 for males) randomly selected in the visceral mass. In females, four categories: oogo- niae, vitellogenic oocytes, ripe oocytes, and atresic oocytes, were considered. In males, the cells were classified into the following three categories: protogoniae	and spermatogoniae, primary and sec- ondary spermatocytes, and, lastly, sper- matids and spermatozoa. The mean per- centage of each cell category was calcu- lated in relation to the total number of cells counted. Mean valúes and corre- sponding S.D. were established for each cell category. For the second study, gonad smears and the determination of sex ratios were made by removing each bivalve from its shell and by rubbing soft masses against a histological slide. The microscopic examination was made using the scale of Lucas (1965) adapted for C. edule by Fernandez-Castro, Guillou, Le Pennec, and CARDENAS López (1989) (see table I). The sex ratio (number of females in relation with the total number of bivalvs with a recognizable sex) was performed when this identifi- cation was easy. A x2 test was used to determine levels of statistical signifi- cance. The condition Índex represents the variations of dry weight for a standard bivalve and aims to elimínate the effect of mollusc growth while revealing an accumulation or a loss of organic matter, associated with reproduction. A single

32

Bergayou ET AL.: Reproduction of Cerastoderma edule in Southwestern Morocco

size class (20-30 mm) was considered and 30 bivalves were randomly chosen to determine this condition Índex. The índex selected was that proposed by Lucas and Beninger (1985): IC = [(dry weight of soft masses) / (dry weight of valves) x 1000]. The dry weight was obtained using a dehydration of soft masses (or shell) in a desiccator (60°C, 24 h).

Population dynamics

To study the dynamics of the popu- lation and to specify the period of juve- nile recruitment, samplings of C. edule were performed from January to December 2002. This study was also carried out in the station 2. Monthly, sixteen sediment samples (surface, 0.0625 m2, height, 20 cm) were collected at low tide according to the method of quadrats used by Elliott and Decamps (1973, in Bayed, 1982). These samples were sieved (square meshes, 1 mm) to recover and count cockles. The antero- posterior length of each cockle was mea- sured using a calliper rule (precisión, 0.1 mm). For mollusc sizes less than 5 mm, a stereomicroscope equipped with a micrometric ocular was used. The indi- vidual valúes recorded for the length of bivalves and sampling dates were com- pared using the FISAT software (Gayanilo, Sparke and Pauly, 1996) to draw size histograms in relation to the frequency of animáis and to make a modal analysis based on the algorithm according to the method by Battacharya (1967). This comparison, with the use of the x2 test (at P<0.05) allows to distin- guish the different size classes in each monthly sample, to determine mollusc densities, and to specify recruitment periods.

Spatial distribution, density and biomass

To determine the spatial distribu- tion, density, and biomass (ash-free dry weight, AFDW) of cockles, two surveys were carried out in 2002 and 2003 (during summer period). The replication of this study during these two periods (in 2002, when the estuary received the

wastewater, and in 2003, when the dis- charge stopped) gives insights on the wastewater pollution impact and the reestablishment of the ecosystem when this pollution stopped. These investiga- tions were made in a total of 8 stations (27 sampling sites) located at 400-500 m intervals from the estuary mouth up to the wastewater outlet (Fig. 1). In each site, four to six sediment samples (surface, 0.0625 m2, height, 20 cm) were collected at low tide according to the method of quadrats used by Elliott and Decamps (1973, in Bayed, 1982). These samples were sieved (square meshes, 1 mm) to recupérate and count cockles, as above.

Ash-free dry weight (AFDW) was determined by dipping molluscs in a solution of 10% HC1 until the shell was completely dissolved. Then, the soft parts were dried for 48 h at 80°C, weighed, placed at 600°C for 2 h and weighed again. The weight loss at 600°C was considered to represent the AFDW of individuáis and was expressed in g/m2 (Bachelet, Bouchet and Lissalde, 1980-1981).

RESULTS

Effects of pollution on the biology of the species

Reproductive cycle: The study of gonad smears from August 2001 to August 2002 had allowed to recognize sex in 1138 bivalves (87.5%). Within this group, the sex ratio of C. edule was 51.1% ± 2.6%, and was well-balanced at 1:1 (x2 = 2.5, P < 0.05). No hermaphro- dite individuáis were found in this pop- ulation. In September, the A stage (undetectable sex) was observed in 75% of cockles and might correspond to a previtellogenic phase rather than a sexual rest, as the percentage of C. edule showing the C stage (gonad maturation) increased in October to reach about 50% in November. The frequency of C stage was above 50% between November and April (Fig. 2A), and subsequently decreased in May (from 75 to 20%), thus corresponding to a slight decrease of the

33

Iberus, 26 (1), 2008

Figure 2. Distribution of sexual-development stages (A) according to the scale of LUCAS (1965) and annual cycle of condition indexes (B) in the populations of C. edule studied from August 2001 to August 2002. The cumulated frequencies of the different sexual-development stages corresponded to the total of bivalves studied (100%). For details of each stage, see Materials and Methods (Table I). Figura 2. Distribución de los estadios de desarrollo sexual (A) según la escala de LUCAS (1965) y ciclo anual de índices de condición (B) en las poblaciones de C. edule estudiadas entre agosto 2001 y agosto 2002. Las frecuencias acumuladas de distintos estadios de desarrollo sexual corresponden al total de bivalvos estudiados ( 1 00%). Véase Material y Métodos (Tabla L) para los detalles de cada estadio.

condition Índex (Fig. 2B). An episode of pardal spawning had thus occurred during this last period. In May, the fre- quency of the D stage (80%) proved that gametogenesis had resumed. In June and July, the C stage was the most fre- quent (65 to 75%) and was followed in August by a more marked decrease of the condition Índex (from 80 to 50 %o) thus indicating an important release of gametes. It may be concluded that two periods of gamete maturation (C stage), the first ranging from November to April and the other occurring in June- July, were differentiated.

The histological study was carried out over a longer period of time (January

2001- March 2002) than the analysis of gonad smears. Mature gonads (IIIA stage) were often observed on more than 50% of cockles studied from January to April (Fig. 3). Episodes of pardal spawn- ing occurred from January to March; fol- lowed by another spawning in April and May (in May, the IIIB stage was noted in 60% of males, Fig. 3A). The reconstitu- tion of the gonad (IIIC stage) is more marked in females (Fig. 3B) in May (80%) and seems more precocious in males. In both sexes, this stage devel- oped in parallel from May to July so that pardal spawning occurred during these months. In August, the IIIB stage was preponderant in both sexes (80% of

34

Bergayou ET AL.: Reproduction of Cerastoderma edule in Southwestern Morocco

A

B

2001 Months 2002

■	Sta	IIID
m	Sta	MIC
El	Sta	IIIB
m	Sta	IIIA
	Sta	II
E	Sta	1
□	Sta	0

■	Sta	IIID
m	Sta	MIC
E	Sta	IIIB
m	Sta	IIIA
a	Sta	II
□	Sta
□	Sta	0

Figure 3. Distribution of gonadic-development stages over 2001-2002 in the males (A) and females (B) of C. edule. The cumulated frequencies of the different developmental stages corresponded to the whole bivalves studied (100%). For details of each stage, see Materials and Methods (Table I). Figura 3. Distribución de los estadios de desarrollo gonadal sobre el periodo 2001-2001 en machos (A) y hembras (B) de C. edule. Las frecuencias acumuladas de distintos estadios de desarrollo sexual corre- sponden al total de bivalvos estudiados (100%). Véase Material y Métodos (Tabla I) para los detalles de cada estadio.

males, 60% of females), proving that the main spawning episode had happened. The resorption of gonads (IIID stage) was observed in a few individuáis after the spawning of May and was less than 25% from June to August. Several females in IIID stage were noted during the other months, but they never exceeded 5%. In September, gametogen- esis started in both sexes (I and II stages were found in 95% of cockles). The mat- uration of the gonad (IIIA stage) was observed in the first bivalves from October to December and partial spawn- ing occurred from November to March.

The highest valúes (2.7) of the gonadic Índex (Fig. 4) were noted

between January and April, thus con- firming the presence of ripe gonads during this period. The lowest valúes (1.7) were found from June to August. In both sexes, the gonadic Índex was always higher than 1 so that the period of sexual rest was short.

Gametogenesis in the population of C. edule: Figure 5 gives the results of stere- ological analysis. From January to March, the percentages of mature gametes increased to peak in April. Another episode of gametogenesis began in May, as demonstrated by the high frequencies of young germinal cells during this month in both sexes. In males, the effect of this developing sper-

35

Iberas, 26 (1), 2008

—°"“a — b

Figure 4. Annual cycle of the gonadic Índex in the males (A) and females (B) of C. edule over 2001-2002.

Figura 4. Ciclo anual del índice gonádico en machos (a) y hembras (b) de C. edule en el periodo 2001- 2002.

matogenesis was high rates of sper- matids and spermatozoa in June or August (grouped frequencies, 75% and 85%, respectively). In females, an impor- tant vitellogenesis was observed in May and June so that the highest frequency of mature oocytes (55%) was noted in July and that of degenerated oocytes (60%) in August. In September, the highest percentages of spermatogoniae (29%) in males and of oogoniae (37%) in females were noted, thus indicating the starting of another gametogenetic wave. From September to December, the gonadic tissue of males was important, as the grouped frequencies of spermato- goniae and of spermatocytes were more than 47%. The same finding was noted in females during this period (grouped rates of oogoniae and of vitellogenic oocytes, >70%). Low percentages of atresic oocytes (5-25%) were always observed in females throughout the year.

From the above study, it can be con- cluded that three successive gametoge- netic waves were differentiated: the first one from January to April, the second one from May to July, and the third one from September to March. Ripe cockles for both sexes were predominant from

January to April, in July, and from January to March.

Population dynamics: The lengths of C. edule , measured from January to December 2002, are given in Figure 6. The period of recruitment spanned from the end of spring to the onset of autumn. The first settlement of juvenile cockles occurred in June. A second cohort appeared in July, a third cohort in August, and a fourth one in October. At the end of autumn, the individuáis recruited in June-July had a length of 18.3 ±1.8 mm and constituted 71.6% of the population. By contrast, those origi- nating from the grouped cohorts of August and October only had a length of 11.1 ± 1.1 mm and represented 9.2% of the population. In addition to these recruitments; a few young cockles (2- 3%) were found for each date of sam- pling. In summer, there was a strong decrease in the number of cockles mea- suring 24.6 ±1.9 mm in length. This diminution is followed by the almost complete disappearance of adult cockles just after the period of recruitment (August 2002) so that the population of C. edule in 2002 was mainly composed of young individuáis which are being renewed each year.

36

BERGAYOU ET AL. : Reproduction of Cerastoderma edule in Sourhwestern Morocco

■ Spz

Hfl Spc

EH3 Spg

B

JFMAMJ JASONDJFM 2001 Months 2002

Figure 5. Frequencies of different cell categories in the male (A) and female (B) gonads of C. edule collected between January 2001 and March 2002. Male line: Spc (primary and secondary sperma- tocytes), Spg (protogoniae and spermatogoniae), Spz (spermatids and spermatozoa) . Female line: D (degenerated oocytes), Og (oogoniae), R (mature oocytes), V (vitellogenic oocytes). The cumu- lated frequencies of the different cell categories corresponded to the whole bivalves studied (100%). Figura 5. Frecuencia de distintas categorías de células en gónadas de machos (A) y hembras (B) de C. edule recolectados entre enero 2001 y marzo 2002. En machos: Spc (Espermatocitos primarios y secun- darios), Spg (protogonias y espermatogonias), Spz (espermatidios y espermatozoos); en hembras: D (ovoc- itos degenerados), Og ( oogonias ), R (ovocitos maduros), V (ovocitos vitelogénicos). Las frecuencias acu- muladas de distintos estadios de desarrollo sexual corresponden al total de bivalvos estudiados (1 00%).

Spatial distribution, biomass, and structure of population of C. edule before and after wastewater discharges

The spatial distribution of C. edule along the estuary, its density and its biomass are given in Table II for the summer surveys (2002 and 2003). During the period of wastewater dis- charge, the species was confined down- stream (stations 1 and 2). By contrast, in 2003, its distribution had extended with an upstream penetration of cockles up to the station 5. The density of C. edule

did not exceed 320 individuals/m2 in 2002, and strongly increased in 2003 to reach valúes higher than 4,900 cockles/m2 in several places (these valúes were found during the periods of recruitment). The mean biomass (AFDW) calculated on the cockle samples collected during summer surveys, increased from 2.54 g/m2 in 2002 to 14.87 g/m2 in 2003.

Table III shows the different groups of cockles constituting the population in summer surveys (2002 and 2003).

37

Iberus , 26 (1), 2008

Length (mm) 0 10 20 30

N=171

N=182

N=207

N=242

N=300

N=244 N=1 14

N=119

N=256

N=92

N=119

Figure 6. Size distribution of C. edule in the estuary of Oued Souss from January to December 2002 and the principal normal components. Month and numbers of individuáis measured (N) are given for each sampling.

Figura 6. Distribución de tallas de C. edule en el estuario del Oued Souss entre enero y diciembre 2002 y componentes normales principales. Meses y número de ejemplares medidos (N) están indicados para cada muestra.

During the wastewater discharges in the estuary (July 2002), individuáis are dis- tributed among four groups: two classes with lowest lengths (6.81 ± 1.53 mm and 9.97 ± 0.83 mm), deriving from a recruit- ment in May and June; and two classes of oíd cockles (24,72 ±2.17 mm and 27.5 ± 0,76 mm). In July 2003, the most fre- quent group (89.2%) was composed of young individuáis (length, 6.55 ± 1.17 mm; 11.76 ± 1.63 mm) originating from a recruitment in May and June. Another group of médium size (36.25 ± 1.73 mm) appeared for the first time and probably comprised cockles more than one year oíd, as the absence of growth lines on cockle valves did not allow to easily identify the different age subgroups constituting this last size group.

DISCUSSION

The results reported in the present study on the gonochorism of C. edule agree with the reports of several authors (Gimazane, 1971; Kingston, 1974). Several cases of accidental hermaphro- dism (4%0) were also noted by Fernan- dez Castro, Guillou, Le Pennec and Cárdenas López (1989). In the estuary of Oued Souss, the sex ratio of cockles was well-balanced so that pollution did not have an influence on the distribu- tion of males and females. This finding agrees with studies that some authors have performed in other populations of C. edule at different latitudes, such as the report by Kingston (1974) along the coasts of Kent (UK), that of Ivell (1981)

38

BERGAYOU ET AL.: Reproduction of Cerastoderma edule in Southwestern Morocco

Table II. Spatial distribution of C. edule along the estuary, its density and its Biomass (AFDWg / m2) during wastewater contamination (summer 2002) and after stopping of pollution (summer

2003).

Tabla II. Distribución espacial de C. edule a lo largodel estuario , su densidad y su biomasa (AFDW/m2) durante vertidos de agua contaminada ( verano 2002) y después de poner fin a la contaminación ( vera- no 2003).

Sfátions	Sampling sites	2002 2003 Density (ind/m2)	2002 2003 Biomass AFDW (g/m2)
0	OB	4		0.0012
	ObisA	8/2		32.368
	ObisB	24		0.08
1	1A	4	0.6492
	IB	4		0.85
	Ibis A	20		1.22
	IbisB	4 24	0.582	3.12
	TA	36		0.446
	TB	16		0.48
2	2A	108		0.28
	2B	6760		102.892
	2bisA	320	5.539
	2bisB	112	3.648
	2'A	4972		83.768
3	3A	8		0.1384
	3'A	432		3.7176
	3'B	636		6.8256
	3B	8		0.0416
4	4'A	16		0.074
	4'B	124		2.0676
5	5B	68		0.5248

in the Limfjord (Denmark), that of Mejuto (1984) in Ria de Pasaxe (Spain), or still that of Fernandez Castro, Guillou, Le Pennec and Cárdenas López (1989) at Brouennou (France).

Through methods used for repro- ductive cycle analysis, complementary and concordant results were noted. In the year, two successive gametogenetic waves, the first occurring from Septem- ber to April and the second in May-July, were differentiated in this population and spawning periods staggered over time. These phenomena can be explained by an effect of latitude (Sola, 1997; Rodriguez-Rua, Prado, Romeo

and Bruzon, 2003) and, in particular, by water temperature (Hugues, 1971). When temperature was less than 10°C, it induced early spawning, followed by gonad reconstitution and a second period of spawning.

The presence of atresic oocytes observed throughout the year during vitellogenesis, as mentioned by Lubet (1991) is apparently a frequent phenom- enon in bivalves noted in the start of gametogenesis (first mature oocytes degenerate), after partial spawnings and in the end of a reproductive cycle.

The long period of cockle recruit- ment (from June to October) in 2002 can

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Iberus, 26 (1), 2008

Table III. Distribution of shell lengths for C. edule during summer surveys (2002 and 2003): prin- cipal normal components.

Tabla III. Distribución de longitudes de conchas de C. edule durante muéstreos de verano (2002 y 2003): principales componentes normales.

Group N°	Percentage (%)	July 2002 Mean of shell length (mm)	Structure of population S.D	Percentage (%)	July 2003 Mean of shell length (mm)	S.D
1	19.5	6.81	1.53	11.4	6.55	1.17
2	16.4	9.9 7	0.83	77.8	11.76	1.63
3	55.5	24.72	2.17	10.68	36.25	1.73
4	8.4	27.5	0.76

be easily explained by spawning which occurred from April to August and this time was perfectly consistent with the gonadic-development stages deter- mined by the histological study of gonads and the examination of gonad smears. Contrary to juveniles recruited in June-July which had a better develop- ment, those settled from August to October showed a great mortality. This last result would not be related to wastewater pollution, in agreement with the reports by Madani (1989), Sauriau (1992), Bachelet, Guillou and Labourg (1992a), or with that by Bachelet, Desprez, Ducrotoy, Guillou, Labourg, Rybarczyk, Sauriau, Elkaim and Glémarec (1992b). According to these authors, high mortalities of cockles were noted in the recruitments which occurred at the end of summer, in autumn, and in winter. This mortality affected small- sized (<10 mm) cockles and may be explained by the almost complete absence of energetic reserves (Sauriau, 1992) whereas the metabolism of young cockles was changing (Gabbott, 1976).

By contrast, the disappearance of medium-sized molluscs in 2002 coin- cided with the period of summer recruitment. This finding might be explained, either by a great predation of cockles by Haematopus ostralegus (this bird only tackled on médium sizes as reported by Atkinson, Clark, Bell, Daré, Clark and Ireland, 2003; John-

stone and Norris, 2000), or by a high rate of mortality for these bivalves, as their vulnerability became more marked with increasing age and was also dependent on the quality of waters and/or an eventual eutrophication in the estuary, as demonstrated by Ducro- toy and Ibanez (2002). Indeed, as sea waters in winter and spring had high loads of mineral seston in the absence of pollution, the filter-feeders produced numerous pseudo-faeces and had a marked energetic expense for selective sorting of particles, mucus secretion, and cleaning of gills for Mytilus edulis (Widdows, Fieth and Worrall, 1979) or for Crassostrea gigas (Héral, 1986). According to Foster-Smith (1975a, b) and Newell (1977), the behaviour of adult cockles was different, as they adapted their pumping activity in the presence of high concentrations of mineral seston, with a passage by a rel- ative State of dormancy (Savari, Lock- wood and Sheader, 1991). However, such a behaviour did not seem to exist during wastewater discharges in summer, as cockles were in reproduc- tion and had to live in waters double loaded with matters in suspensión (pol- lution) and the phyto-planktonic bloom (with the increase of temperature), therefore placing these bivalves under stress conditions and inducing a high mortality.

Since November 2002, the discharge of decanted wastewater in another site

40

Bergayou ET AL. : Reproduction of Cerastoderma edule in Southwestern Morocco

beyond the estuary and the conversión of this ecosystem into a marine environ- ment had resulted, for C. edule, in a wider spatial distribution, a strong increase of density, and the appearance of médium sizes in this site. To comment on these changes, it is neces- sary to take into account the reproduc- tion of cockles living in this estuary, as it is stretched over all the year. Indeed, according to Gordo (1982), the repro- ductive cycle of Spanish and Portuguese populations of C. edule showed a period of sexual rest during summer months and the author explained it by the mean temperature of sea water which were more than 28°C and would inhibit the

BIBLIOGRAPHY

Ansell, A. D., Barnett, P. R. O., Bodoy, A. and Masse, H., 1981. Upper temperature toler- ances of some European molluscs. III. Cardium glaucum, C. tuberculatum and C. ed- ule. Marine Biology, 65: 177-183.

Atkinson, P. W., Clark, N. A., Bell, M. C., Daré, P. J., Clark, J. A. and Ireland, P. L., 2003. Changes in commercially fished shell- fish stocks and shorebird populations in the Wash, England. Biological Conservation, 114: 127-141.

Bachelet, G., Bouchet, J. M. and Lissalde, J. P., 1981. Les peuplements benthiques de la Gironde: biomasse, productivité et évolu- tion structurale. Oceanis, 6: 593-620.

Bachelet, G., Guillou, J., Labourg, P. J., 1992a. Adult, larval and juvenile interactions in the suspension-feedingbivalve, Cerastoderma ed- ule: field observations and experiments. In Colombo, G., Ferrari, I., Ceecherelli, V.U., and Rossi, R., (Eds.): Marine eutrophisation and population dynamics. Fredensborg, 175- 182.

Bachelet, G., Desprez, M., Ducrotoy, J. P., Guillou, J., Labourg, P. J., Rybarczyk, H., Sauriau, P. G., Elkaim, B. and Glé- marec, M., 1992b. Role de la compétition intraspécifique dans la régulation du re- crutement chez la coque, Cerastoderma edule (L). Anuales de l'Institut Océanographique, 68:75-87.

Battacharya, C. G., 1967. A simple method of resolution of a distribution into Gaussian components. Biometrics, 23: 115-135.

Bayed, A., 1982. Ecologie descriptive et dynamique des plages de la región de Rabat, Maroc. Doctoral Thesis, Brest, 122 pp.

reproduction of this species, as they were cióse from the lethal temperature recorded for C. edule (Ansell, Barnett, Bodoy and Masse, 1981). As the cockles from the estuary of the Oued Souss river practically did not have sexual rest and showed a gametogenesis starting towards autumn, the results noted in this site might be interpreted as an adaptation of this cockle population to high temperatures of sea waters which exist in the South of Morocco. Under these conditions, it is logical to consider C. edule an opportunistic species which might quickly overtake new areas in presence of favourable environmental conditions.

Ducrotoy, J. P. and Ibanez, F., 2002. Ecolog- ical groups of estuarine macrobenthic in- vertebrates in the Baie de Somme (France): changes in time and space. Journal ofthe Ma- rine Biological Association of the United King- dom, 5: 749-769.

Fernández-Castro, N., Guillou, J., Le Pen- nec, M. and Cárdenas López, J. J., 1989. Le cycle sexuel de Cerastoderma edule L. (Bivalve: Cardiidae) á Brouennou (Finistére). Haliotis, 19: 325-334.

Foster-Smith, R. L., 1975a. The effect of con- centration of suspensión on the filtration rates and pseudofaecal production for Mytilus edulis (L.), Cerastoderma edule (L.) and Venerupis pul- lastra (Montagu). Journal of Experimental Marine Biology and Ecology, 17: 1-22.

Foster-Smith, R. L., 1975b. The role of mucus in the mechanism of feeding in three filter- feeding bivalves. Proceedings of the Malaco- logical Society ofLondon, 41: 571-588.

Gabbott, P. A., 1976. Energy metabolism. In Bayne, P. A. (Ed.): Marine mussels: ecology and physiology. Cambridge University Press, Cambridge, 213-355.

Gabe, M., 1968. Techniques histologiques. Masson et Cié, Paris, 1113 pp.

Gayanilo, F. C. Jr., Sparke, P. and Pauly, P., 1996. FISAT Software. FAO-ICLARM-Stock- Assessment-Tools, Makati City, Metro Manila, The Philippines.

Gimazane, J. P., 1971. Introduction a Vétude ex- périmentále du cycle sexuel d’un mollusque Bi- valve Cardium edule L. Analyse des populations, évolution de la gonade et action de quelquesfac- teurs: nutrition, température, photopériode. Doc- toral thesis, University of Caen, 112 pp.

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Iberus, 26 (1), 2008

Gordo, L. S., 1982. Aspects of the growth and density of Cerastoderma edule in the Alvor Salt Marsh, South Portugal. Arquivos do Museu Bocage (Series A), 19: 435-452.

Guillou, J., Bachelet, G. and Glémarec, M., 1992. Influence des fluctuations de tem- pérature sur la reproduction et le recrute- ment de la coque Cerastoderma edule (L). An- uales de l'Institut Océanographique , 68: 65-74

Héral, M., 1986. L'ostréiculture frangaise tra- ditionnelle. In Barnabe, G., (Ed): Aquacul- ture, 2nd ed. Lavoisier, París. 345-390.

Hugues, R. N., 1971. Reproduction of Scrobic- ularia plana Da Costa (Pelecypoda: Semelidae) in North Wales. The Veliger, 14: 77-81.

Ivell, R., 1981. A quantitative study of a Ceras- toderma-Nephthys community in the Lim- fjord, Denmark, with special reference to production of Cerastoderma edule. Journal of Molluscan Studies, 47: 147-170.

Johnstone, I. and Norris, K., 2000. The influ- ence of sediment type on the aggregative re- sponse of oystercachers, Haematopus ostrale- gus, searching for cockles, Cerastoderma edule. Oikos, 89: 146-154.

Kingston, P. F., 1974. Studies on the repro- ductive cycles of Cardium edule and C. glau- cum. Marine Biology, 28: 317-323.

Lubet, P., 1991. Reproduction des mollusques In Barnabé, G., (Ed.): Bases biologiques et écologiques de l'aquaculture. Lavoisier, Tec and Doc, París, 167-210.

Lubet, P., 1959. Recherches sur le cycle sexuel et l'émission des gamétes chez les Mytilidés et les Pectinidés. Doctoral Thesis, University of París, 159 pp.

Lucas, A., 1965. Recherches sur la sexualité des Mollusques Bivalves. Bulletin Biologique de Trance et de Belgique, 99: 115-247.

Lucas, A. and Beninger, P. G., 1985. The use of physiological condition indices in marine bivalve aquaculture. Aquaculture, 44: 187- 200.

Madani, I., 1989. Dynamique des populations et processus de recrutement chez quatre espéces de bivalves appartenant aux genres Abra et Ceras- toderma, dans le bassin d'Ar cachón. Doctoral Thesis, University of Bordeaux 1, 152 pp.

Mejuto, J., 1984. Primeros datos sobre la di- námica de la poblation de Cerastoderma edule L.) de la Ria do Pasaxe ( NW de Galicia), es- trategias de explotation. Actas IVo Simposio Ibérico de Estudos do Benthos Marinho, 2: 83-102.

Newell, R. I. E., 1977. The ecophysiology of Cardium edule (Linné). Ph. D. Thesis. Uni- versity of London, 250 pp.

Rodríguez-Rua, A., Prado, M. A., Romeo, Z. andBruzon, M., 2003. The gametogenic cy- cle of Scrobicularia plana (Da Costa, 1778) (Mollusca: Bivalvia) in Guadalquivir estu- ary (Cádiz, SW Spain). Aquaculture, 217: 157- 166.

Sauriau, P. G., 1992. Les mollusques benthiques du bassin de Marennes-Oléron: estimation et cartographie des stocks non cultives, compétition spatiale et trophique, dynamique de population de Cerastoderma edule (L.). Doctoral Thesis, University of Nantes, 262 pp.

Savari, A., Lockwood, A. P. M. and Sheader, M., 1991. Variations in the physiological State of the common cockle ( Cerastoderma edule (L.)) in the laboratory and in Southampton Water. Journal of Molluscan Studies, 57: 33-44.

Seed, R., 1975. Reproduction in Mytilus edulis L. (Mollusca: Bivalvia) in European waters. Pubblicazioni delta Stazione Zoológica di Napoli, 39: 317-334.

Seed, R. and Suchanek, T. H., 1992. Popula- tion and community ecology of Mytilus. Chapter 4. In Gosling, E., (Ed.): The mussel Mytilus: ecology, physiology, genetics and cul- ture. Developments in Aquaculture and Fish- eries Science, n° 25. Elsevier, Amster- dam/New York, 87-168.

Sola, J. C., 1997. Reproduction, population dy- namics growth, and production of Scrobicu- laria plana Da Costa (Pelecypoda) in the Bida- soa estuary, Spain. Netherlands Journal of Aquatic Ecology, 30: 283-296.

Widdows, J., Donkin, P., 1992. Mussels and environmental contaminants: bioaccumula- tion and physiological aspects. In Gosling, E., (Ed.): The mussel Mytilus: ecology, physiology, genetics and culture. Developments in Aqua- culture and Fisheries Science, n° 25. Elsevier, Amsterdam/New York, 383-424.

Widdows, J., Fieth, P. and Worrall, C. M., 1979. Relationship between seston, available food and feeding activity in the common mussel Mytilus edulis. Marine Biology, 50: 195- 207.

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Iberus , 26 (1): 43-46, 2008

Xylodiscula wareni n. sp., una nuova specie per le coste orientali della Sicilia

Xylodiscula wareni n. sp., una nueva specie para las costas orientales de Sicilia

Cesare BOGI* e Stefano BARTOLINI**

Recibido el 27-X-2007. Aceptado el 15-XII-2007

RIASSUNTO

Si descrive un piccolo gasteropode planispirale, che non corrisponde a nessuna delle spe- cie attualmente viventi nel Mar Mediterráneo, trovato in campioni di sedimento raccolti a profonditá cómprese tra i 35 e i 52 m lungo le coste siciliane. La forma generóle della conchiglia ci ha indotto ad ascrivere questa specie, solo prowisoriamente, al genere Xylo- discula Marshall, 1988 anche se alcune caratteristiche della protoconca, non iperstrofica, lo escluderebbero.

Questa specie si descrive come nuova, con il nome di Xylodiscula wareni anche se proba- bilmente non appartiene a questo genere, evitando di descrivere al momento un nuovo genere scarsamente definito.

ABSTRACT

A small planispiral gastropod, which could not be ascribed to any known species from the Mediterranean or adjacent seas, was found in sediment samples collected in depths between 35 and 52 m in the seas around Sicily.

The general shape resmbles the genus Xylodiscula Marshall, 1 988, but the protoconch ¡s not heterostrophic and has a distinct sculpture not described from any gastropod. There- fore we describe this new species as Xylodiscula wareni, although it probably does not belong to the genus, instead of creating a new, poorly defined genus.

RESUMEN

Se describe un pequeño gasterópodo planiespiral recolectado entre 35 y 52 m de profun- didad en las costas Sicilianas, que no pudo ser asignado a ninguna especie conocida del Mediterráneo ni de mares adyacentes. La forma general se asemeja al género Xylodiscula Marshall, 1 988, aunque la protoconcha no sea heterostrófica y tenga una escultura dis- tinta que no se conoce en ningún otro gasterópodo. Se propone como nueva especie Xylodiscula wareni. Aunque probablemente no pertenezca a este género, se descarta de momento la descripción de un género nuevo escasamente definido.

PAROLE CHIAVE: Gastropoda, Xylodisculidae, Xylodiscula wareni, nuova specie, Mar Mediterráneo, recente. KEY WORDS: Gastropoda, Xylodisculidae, Xylodiscula wareni , new species, Mediterranean Sea, recent. PALABRAS CLAVE: Gastropoda, Xylodisculidae, Xylodiscula wareni , nueva especie, mar Mediterráneo, reciente.

* Via delle Viole 7 1-57124, Livorno. e-mail bogicesare@tiscali.it

** Via E. Zacconi,l6 1-50137, Firenze. e-mail stefmaria.bartolini@libero.it

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Iberus , 26 (1), 2008

INTRODUZIONE

Le nostre continué ricerche malaco- logiche e Pesame di numerosi campioni di sedimento raccolti lungo le coste della Sicilia Nord-Orientale e le isole antistanti, ci ha portato, questa volta, a studiare alcuni micromolluschi, in tutto quattro esemplari, isolati da piccole

quantitá di detrito raccolto a profonditá variabili tra i 35 mt. e i 52 mt.

II piccolo gasteropode di forma pla- norbide viene, per l'aspetto generale della conchiglia, solo provvisoriamente attribuito al genere Xylodiscula Marshall, 1988, in quanto le caratteristiche della sua protoconca, non iperstrofica, lo escluderebbero .

SISTEMATICA

Ordine Heterostropha Fischer P. , 1885 Famiglia Xylodisculidae Waren A., 1992 Genere Xylodiscula Marshall,1988

Xylodiscula wareni n. sp. (Fig. 1)

Materiale esaminato: 1 esemplare (olotipo, fig.l a-e) proveniente da detriti raccolti nel Luglio 2005 alia base della "Secca dei 6 metri" presso l'isola di Filicudi a -50 m. , 1 esemplare (paratipo A) rac- colto nel Giugno 2006 a Cannizzaro, loe. Bellatrix, -35 m.di profonditá lungo una párete rocciosa, 2 esemplari (paratipi B e C) provenienti da campioni di detriti coralligeni raccolti a Scilla a -52 m. Materiale tipo: L'olotipo (Diam.= 1.1 mm), (Fig. 1A-E ) é stato depositato nella collezione malaco- logia del Museo di Storia Naturale del Mediterráneo di Livorno, Italia, con il numero: Malacologia Vol. V, n. 734. 1 paratipi sono conservad nelle seguenti collezioni: il paratipo A (Diam.= 1.0 mm), nella collezione di S. Bartolini (Firenze), il paratipo B (Diam.= 1,3 mm) , e il paratipo C (Diam.= 1,2 mm), nella collezione E. Perna (Napoli).

Locus typicus: Detriti raccolti alia base della "Secca dei 6 metri" presso Pisóla di Filicudi a -50 m. di profonditá.

Etimología: La specie é stata dedicata al Dottor Anders Warén, malacologo di fama mondiale e specialista, tra l'altro, nei piccoli "Skeneimorpha".

Diagnosi (olotipo): Conchiglia piccola, fragüe, trasparente, di forma planor- bide.La protoconca (fig.l e) é costituita da 0.7 giri di spira di cui la parte iniziale é scolpita da piccole e irregolari depres- sioni.La teleoconca é costituita da circa 2 giri di spira attraversati da deboli linee di accrescimento. I giri si toccano solo per un breve tratto piú o meno alia peri- feria del giro precedente e quindi la sutura risulta profonda e leggermente canaliculata. Spira arrotondata con la protoconca di poco sporgente nella parte superiore della stessa. Alia base della conchiglia é ben visibile per tutta la lunghezza della teleoconca, una evi- dente carena posizionata internamente all'ombelico. La bocea é di forma roton- deggiante con la parte inferiore legger- mente espansa in prossimitá della carena. La larghezza dell'ombelico é

circa il 30% del diámetro delPintera con- chiglia.

Dimensioni : Diámetro^ 1.1 mm.

Opercolo e partí molli ancora scono- sciute.

Distribuzzione: La specie sembra avere una distribuzione ristretta a poche localitá delle coste siciliane, ed il suo habitat non sembra essere mai superfi- ciale.

Discussione : L'attribuzione di questi esemplari al genere Xylodiscula é da rite- nersi provvisoria in quanto solo lo studio delle partí molli potranno dame un'inquadramento tassonomico piú congeniale. La forma generale della con- chiglia in realtá corrisponde alie caratte- ristiche tipiche di questo genere, ma la protoconca differisce in quanto non ha uno sviluppo iperstrofico típico della famiglia Xylodisculidae Warén, 1992.

44

Bogi E BartolinI: Xylodiscula wareni n.sp., una nuova specie per le coste della Sicilia

Figura 1. Xylodiscula wareni n. sp., Filicudi -50 m, olotipo (Museo di Storia Naturale del Mediter- ráneo di Livorno, Coll. Malac. N° Malacologia Vol. V n. 734). A: vista dall’alto; B: vista basale; C: vista frontale; D: dettaglio dell’ombelico; E: dettaglio della protoconca.

Figura 1. Xylodiscula wareni n.sp., Filicudi -50 m, holotype (Museo di Storia Naturale del Mediterrá- neo di Livorno, Coll. Malac. N° Malacologia Vol. V n. 734). A: apical view; B: basal view; C: frontal view; D: detail ofthe umbilicus; E: detall ofthe protoconch.

II genere Xylodiscula é attualmente rappresentato nel Mar Mediterráneo da due specie: X. boucheti Warén, Carrozza e Rocchini, 1992, e X. leus Warén, 1992.

Warén stesso nel suo articolo (Warén, 1992) evidenzia la difficoltá nel distin- guere le due specie che differiscono quasi esclusivamente per il diámetro

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Iberus, 26 (1), 2008

dell'ombelico che é il 30-33 % del diáme- tro deH'intera conchiglia in X. boucheti mentre in X. lens é il 40%. La caratteri- stica principale che distingue X. wareni da queste due specie, come dalle altre non mediterranee appartenenti a questo genere, oltre alia diversa protoconca, é la presenza di una carena ben visibile alia base della conchiglia (Fig. IB).

Abbiamo dubitato che gli esemplari potessero appartenere ad una specie dulciacquicola o terrestre, ma le nostre ricerche e l'opinioni di alcuni specialisti hanno escluso questa possibilitá.

RINGRAZIAMENTI

Un particolare ringraziamento al Dottor Ánders Warén del Museo Svedese di Storia Naturale di Stoccolma, per aver eseguito le foto al SEM e per i consigli dati nella rilettura critica dell' articolo, e all'a-

BIBLIOGRAFIA

Marshall, B.A., 1988. Skeneidae, Vitrinelli- dae and Orbitestellidae (Mollusca: Gastro- poda) associated with biogenic substraía from bathyal depths off New Zealand and New South Wales. Journal of Natural History, 22: 949-1004.

La specie tipo del genere, Xylodi- scula vitrea Marshall, 1988, come puré X. eximia Marshall, 1988, originarle rispetti- vamente dell'Australia e della Nuova Zelanda, sono state tróvate su pezzi di legno affondati ed anche le specie descritte da Warén per il Mar Mediterrá- neo sono state raccolte viventi in un biotopo caratterizzato da fibre di Posido- nia e frammenti di legno affondati.

Nei campioni di sedimento dove noi abbiamo trovato i pochi esemplari di X. wareni, non erano presenti frammenti di Posidonia.

mico Edoardo Perna per aver messo a disposizione i suoi esemplari nonché le foto degli stessi. All'amico Ivano Niero per aver studiato gli esemplari come even- tuali appartenenti alia fauna continentale.

Warén A., 1992. New and little known "Ske- neimorph" gastropods from the Mediterra- nean Sea and the adiacent Atlantic Ocean. Bol- lettino Malacologico, 27 (10-12):149-248.

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Iberus , 26 (1): 47-51, 2008

The colour white diminishes weight loss during aestivation in the arid-dwelling land snail Sphincterochila (Albea) can - didissima

El color blanco disminuye la pérdida de peso durante la estivación en el caracol de medios áridos Sphincterochila (Albea) candidissima

Gregorio MORENO-RUEDA*

Recibido el 14-V-2007. Aceptado el 2-1-2008

ABSTRACT

It has been suggested that white colour is beneficial for snails living ¡n arid environments. In this work, shell coloration in the arid-dwelling land snail Sphincterochila (Albea) can- didissima was manipulated during aestivation. Snails painted black lost more body weight than did control ones, presumably as a consequence of higher heat absorption. This sug- gests that light colour is advantageous for this land snail.

RESUMEN

Se ha sugerido que el color blanco es beneficioso para los caracoles en ambientes ári- dos. En el presente trabajo se manipula la coloración de la concha en el caracol de medios áridos Sphincterochila (Albea) candidissima durante la estivación. Los caracoles pintados de negro perdieron más peso que los caracoles que sirvieron como control, pre- sumiblemente como una consecuencia de una mayor absorción de calor. Esto sugiere que los colores claros son ventajosos para este caracol.

KEY WORDS: Sphincterochila candidissima , arid environments, colouration. PALABRAS CLAVE: Sphincterochila candidissima , medios áridos, coloración.

INTRODUCTION

It is well established that tegument colour has important functions in camou- flage, as well as in communication (e.g., Badayev and Hill, 2000; Théry, Debut, Gómez and Casas, 2005; Exnerova, SVADORA, BARCALOVA, LANDOVA,

Prokopova, Fuchs and Socha, 2006). The colour of teguments depends on the wavelengths that are reflected. Therefore, colouration affects the energy that is

absorbed by the tegument, the amount being higher as the colour darkens. In this sense, animal colouration may also have a role in thermoregulation, espe- cially important for arid-dwelling animáis (Cloudsley-Thompson, 1978). Terrestrial molluscs are very susceptible to dehydration (Prior, 1985; Luchtel and Deyrup-Olsen, 2001), and therefore need adaptations to survive in arid envi-

* Konrad Lorenz Institut für Vergleichende Verhaltensforschung, Ósterreischische Academie der Wissenschaften, SavoyenstraEe la, A- 1160, Wien (Austria) and Departamento de Biología Animal, Facultad de Ciencias, Universidad de Granada, E- 18071, Granada (Spain).

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Iberus , 26 (1), 2008

ronments. White colour may favour the success of land-snails in warm environ- ments: White shells have a higher reflectance of sunlight (Schmidt- Nielsen, Taylor and Shkolnik, 1971), and, as a consequence, land snails with light-coloured shells register lower body temperatures (Heath, 1975), thereby improving survival under high tempera- tures (Richardson, 1974). This translates as a selective pressure for whiter shells in arid environments and, in fact, some studies have correlated shell colour with environment temperature (Jones, 1973; but there are exceptions: Heller, 1984).

The snails of the genus Sphincterochila have white shells. In Sierra Elvira (SE Spain), Sphincterochila (Albea) candidísi- ma (Draparnaud, 1801) is the most abun- dant gastropod (Moreno-Rueda, 2002). Sierra Elvira has an arid environment, and sheltering in protective microhabi- tats may be a vital strategy against dehy- dration (Steinberger, Grossman, Du- binsky and Shachak, 1983; Arad, Goldenberg and Heller, 1989; Cook, 2001). However, S. candidísima does not use refuges during drought periods (spring and summer) (Moreno-Rueda, 2007; Moreno-Rueda and Collantes- Martín, 2007). Because the shell of S. candidísima is puré white, I hypothe- sized that shell colour might contribute to the survival of S. candidísima in Sierra Elvira, explaining why this snail does not need refuges against dehydration. I investigated this hypothesis by manipu- lating the shell colour of S. candidísima during aestivation (painting some snails), and by examining the effect of this manipulation on the amount of body mass lost. About 80-90% of fresh body weight (shell not included) of Sphincterochila land snails is water, and, therefore, a decrease in body weight sug- gests a loss of water (Schmidt-Nielsen et al., 1971; Yom-Tov, 1971; Steinberg- er, Grossman and Dubinsky, 1981).

METHODS

This study was performed in Sierra Elvira (SE Spain, 37° 15' N, 3o 40' W), a

small mountain range with a dry mesomediterranean climate (UNESCO, 1963). The study area undergoes five months of drought each year, with an averáge annual precipitation of 600-1000 mm (Alonso, López- Alcántara, Rivas and IbáÑez, 1985). It is, therefore, a dry zone for land snails. Table I presents cli- matic data during the study period, measured from the meteorological station of Pinos Puente, about three kilo- metres from the study area, and approx- imately at the same altitude (630 m. a.s.l.).

Sphincterochila candidísima is the only species of the genus Sphincterochila in Sierra Elvira (Ruiz Ruiz, Cárcaba Pozo, Porras Crevillén and Arrébola Burgos, 2006). In the study area, this species begins aestivation in April-May (Moreno-Rueda, 2007; Moreno-Rueda and Collantes- Martín, 2007). This snail adheres to rock or vegetation during aestivation. For manipulation, snails were not sepa- rated from the substrate, because this could provoke dehydration in the snails (Luchtel and Deyrup-Olsen, 2001). For this reason, I could not measure body mass before treatment, but I col- lected 75 additional individuáis in order to analyse the relationship between shell morphology and body mass. The experiment started on 26 June 2005. Each individual found was sequentially assigned to the control group (C), to the control of manipula- tion group (CM), or to the experimental group (E). Manipulation in control group was only a mark for recognition. Snails in the CM group were painted in yellow with a marker. Paint covered approximately 50% of shell surface. In the experimental group, the shell was painted black with a marker in the same way as in CM group. In total, 52 snails were used in each group (n = 156). The study area was prospected two months later (26 August 2005). Snails found were collected and mea- sured (shell height and width) with a calliper (accuracy 0.01 mm.) and weighed with a digital balance (accu- racy 0.1 g.).

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MORENO Rueda: Colour white and aestivation weight loss in Sphincterochila candidissima

Table I. Climatic data of the meteorological station of Pinos Puente, located near of the study area, for the study period (06/26/2005 to 08/26/2005).

Tabla I. Datos climáticos de la estación meteorológica de Pinos Puente, próxima a la zona de estudio, para el período de estudio (2610612005 a 26/08/2005).

	Mean	S.E.	Mínimum	Máximum
Daily maximal íemperature (9C)	36.8	0.36	30.7	42.9
Daily minimal temperature (9C)	17.6	0.30	12.7	22.8
Average daily temperature (9C)	27.0	0.27	23.4	31.3
Daily radiation (MJ/m2)	27.6	0.51	13.9	32.5
Daily precipitation (mm.)	0.03	0.02	0.00	0.80
Table II. Average weight	on the day 08/26/2005, and shell height	and width for the snails in the
experimental (E), control (C) and control of	manipulation (CM)	groups. The last	row shows the

average weight after statistically controlling for shell height and width. The last column shows the results of ANOVA and ANCOVA. In brackets is the standard error.

Tabla II. Peso promedio el día 26/08/2005, y altura y anchura de la concha para los caracoles en el grupo experimental (E), control (C) y control de la manipulación ( CM). La última fila muestra el peso promedio después de controlar estadísticamente por la altura y anchura de la concha. La última columna muestra los resultados de los tests de ANOVA y ANCOVA. Entre paréntesis el error estándar.

	E group n= 29	C group n= 34	CM group /7 = 30	F	ANOVA d.f.	P
Weight (g.)	2.70 (0.09)	3.02 (0.09)	2.87 (0.09)	3.15	2, 90	<0.05
Width (mm.)	21.49 (0.22)	21.31 (0.21)	21.33 (0.22)	0.21	2, 90	0.81
Height (mm.)	16.54 (0.18)	16.77 (0.17)	16.37 (0.18)	1.33	2, 90	0.27
Weight (controlled for shell size)	2.69 (0.07)	3.00 (0.06)	2.91 (0.07)	6.28	2, 88	<0.003

The variables had a distribution similar to normal (Kolmogorov-Smirnov test, p > 0.05), and parametric statistics were used. An ANOVA was used to test the effect of the treatment on body weight, and an ANCOVA was used con- trolling by snail body size (height and width). For post hoc comparisons the Fisher LSD test was used. The Chi- square was used to test the probability of survival according to treatment.

RESULTS

In August, I recaptured 34 snails alive in the control group, 30 for the CM group, and 29 of the experimental group. The frequency of recaptures did not differ significantly between the three

groups (x22= 1.12; p= 0.57). When indi- viduáis were collected in August, there were significant differences for body mass between the treatments (Table II). Individuáis of the experimental group weighed less than those in the control one (post hoc Fisher LSD, p = 0.01), while the average weight in the CM group was intermediate between the other two groups (post hoc, CM vs. C, p = 0.22; CM vs. E, p = 0.22). In the addi- tional sample of 75 individuáis, body mass was strongly predicted by shell morphology (Múltiple Regression Model; R2 = 0.81; F 2,72 = 149.0; p < 0.001; equation: Body mass = -5.16 (SE = 0.46; t72 = 11.2) + 0.28 (SE = 0.03; t72 = 10.2) x Width + 0.14 (SE = 0.03; t72 = 5.1) x Height). There were no significant dif- ferences for body size (height and

49

Iberus , 26 (1), 2008

width) between the three groups (MANOVA, Wilks = 0.94; F4, ízs = 1.46; p = 0.22; Table II), suggesting that initial body mass did not differ among groups. When the analyses were repeated with shell height and width as a covariate, differences in weight between groups were accentuated (ANCOVA, Vi, 88 = 6.28; p < 0.003; Height effect: Fi, 88 = 10.90; p = 0.001; Width: Fi,88 = 21.98; p < 0.001; Table II). Differences between the control group and the experimental group increased in this analysis (post hoc, p < 0.001), while body weight in the CM group remained intermediate between the other two groups (CM vs. C, p = 0.08; CM vs. E, p = 0.08).

DISCUSSION

The findings of this experimental study show that shell colour alteration in Sphincterochila candidissima during aestivation had effects on weight loss, snails with shells painted black suffer- ing a quicker loss of weight than control snails. The most probable mechanism behind this result is that light reflection was lower in shells painted in black, and for this reason they trapped more heat, as shown in other studies with other species of snails (e.g., Heath, 1975). The higher the body temperature, the higher the water loss, decreasing body weight (Yom-Tov, 1971). Body size may affect the interaction between shell colour and heat absorption (Slotow, Goodfriend and Ward, 1993), but there were no differences in body size between the groups, and dif- ferences in weight remained significant after controlling statistically for shell morphology. This weight loss presum- ably harms fitness, increasing the risk of mortality, especially for the smallest individuáis (with less reserves), or in very dry years (Richardson, 1974). Moreover, the treatment lasted only two months (although the warmest), but S. candidissima aestivates for 5-7 months in the study area (Moreno-Rueda and Collantes-Martín, 2007), and there- fore, the effect should be more accentu-

ated if the entire aestivation period is considered.

The control of manipulation (CM) group, with shells painted in yellow, had weight valúes intermediate to the other two groups. In fact, this group is not a true control of manipulation, as colour was altered with respect to unmanipulated snails. Because their shells were darker than shells in the control group, but lighter than shells in the experimental group, the results support that weight loss is due to shell colour. As weight for the CM group was intermediate, if there was an effect of paint on weight, this cannot completely explain the differences between the control and the experimental group.

Therefore, results presented here and in the literature strongly suggest that the white colour is advantageous for survival in arid-dwelling snails. The question arises as to why white colour is not more widespread in arid environ- ments (see, for example, Heller, 1984). Other selective mechanisms besides thermal selection act on shell colour, such as predation (Jones, Leith and Rawlings, 1977). Lighter shells, espe- cially those with a puré white colour as in Sphincterochila candidissima , are usually easier to detect by predators (Reed and Janzen, 1999). However, predation on Sphincterochila candidissima is rare due to its thick shell (Yanes, Suárez and Manrique, 1991), and thus the absence of a strong selection by predators in this species would favour the maintenance of puré white shells.

In conclusión, this study, applying an experimental approach, supports the hypothesis that shell colour affects weight loss in arid-dwelling land-snails, and, as a consequence, fitness, by a mechanism mediated by thermoregula- tion.

ACKNOWLEDGEMENTS

Carlos Marfil Daza and José Luís Ros Santaella collaborated in the field work. David Nesbitt improved the English.

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MORENO Rueda: Colour white and aestivation weight loss in Sphincterochila candidissima

BIBLIOGRAPHY

Alonso, M. R., López- Alcántara, A., Rivas, P. and IbáÑEZ, M., 1985. A biogeographic study of Iberus gualtierianus (L.) (Pulmonata: Helicidae). Soosiana, 13: 1-10.

Arad, Z., Goldenberg, S. and Heller, ]., 1989. Resistance to desiccation and distribution pattems in the land snail Sphincterochila. Jour- nal ofZoology, 218: 353-364.

Badyaev, A. V. and Hill, G. E., 2000. Evolu- tion of sexual dichromatism: contribution of carotenoid- versus melanin-based coloration. Biological Journal of the Linnean Society, 69: 153-172.

Cloudsley-Thompson, J. L., 1978. Adaptive function of the colour s of desert animáis. Comparative Physiological Ecology, 1: 109-120.

Cook, A., 2001. Behavioural ecology: On doing the right thing, in the right place at the right time. In Barker, G. M. (Ed.): The Biology ofTer- restrial Molluscs. CAB International. Walling- ford. Pp. 447-487.

Exnerova, A., Svadora, K., Barcalova, S., Landova, E., Prokopova, M., Fuchs, R. and Socha, R., 2006. Importance of colour in the reaction of passerine predators to aposematic prey: experiments with mutants of Pyrrhocoris apterus (Heteroptera). Biological Journal ofthe Linnean Society, 88: 143-153.

Heath, D. J., 1975. Colour, sunlight and inter- nal temperatures in the land-snail Cepaea nemoralis (L.). Oecologia, 19: 29-38.

Heller, J., 1984. Shell colours of desert land- snails. Malacologia, 25: 355-359.

Jones, J. S., 1973. Ecological genetics and natural selection in molluscs. Science, 182: 546-552.

Jones, J. S., Leith, B. H. and Rawlings, P., 1977. Polymorphism in Cepaea: a problem with too many Solutions? Annual Review in Ecology and Systematics, 8: 109-143.

Luchtel, D. L., Deyrup-Olsen, I., 2001. Body wall: form and function. In Barker, G. M. (Ed.): The Biology ofTerrestrial Molluscs. CAB International. Wallingford. Pp. 147-178.

Moreno-Rueda, G., 2002. Selección de hábitat por Iberus gualtierianus, Rumina decollata y Sphincterochila candidissima (Gastropoda: Pul- monata) en una sierra del sureste español. Iberus, 20: 55-62.

Moreno-Rueda, G., 2007. Refuge selection by two sympatric species of arid-dwelling land snails: Different adaptive strategies to achieve the same objective. Journal of Arid Enviro- ments, 68: 588-598.

Moreno-Rueda, G. and Collantes-Martín, E., 2007. Ciclo anual de actividad del caracol Sphincterochila (Albea) candidissima (Dra- pamaud, 1801) en un medio semiárido. Iberus, 25: 49-56.

Prior, D. ]., 1985. Water-regulatory behaviour in terrestrial gastropods. Biological Reviews, 60: 403-424.

Reed, W. L. and Janzen, F. J., 1999. Natural selection by avian predators on size and colour of a freshwater snail ( Pomacea flage- llata ). Biological Journal of the Linnean Society, 67: 331-342.

Richardson, A. M. M., 1974. Differential cli- ma tic selection in natural population of land snail Cepaea nemoralis. Nature, 247: 572-573.

Ruiz Ruiz, A., Cárcaba Pozo, A., Porras Cre- villen, A. I. and Arrebola, J. R., 2006. Guía de los caracoles terrestres de Andalucía. Fun- dación Gypaetus, Seville.

Schmidt-Nielsen, K., Taylor, C. R. and Shkolnik, A., 1971. Desert snails: problems of heat, water and food. Journal of Experi- mental Biology, 55: 385-398.

Slotow, R., Goodfriend, W. and Ward, D., 1993. Shell colour polymorphism of the Negev desert landsnail, Trochoidea seetzeni: the importance of temperature and predation. Journal of Arid Environments, 24: 47-61.

Steinberger, Y., Grossman, S. and Dubinsky, Z., 1981. Some aspects of the ecology of the desert snail Sphincterochila prophetarum in re- lation to energy and water flow. Oecologia, 50: 103-108.

Steinberger, Y., Grossman, S., Dubinsky, Z. and Shachak, M., 1983. Stone microhabitats and the movement and activity of desert snails, Sphincterochila prophetarum. Malaco- logical Review, 16: 63-70.

Théry, M., Debut, M., Gómez, D. and Casas, J., 2005. Specific color sensitivities of prey and predator explain camouflage in differ- ent visual Systems. Behavioral Ecology, 16 : 25- 29.

UNESCO, 1963. Recherches sur la zone aride. Etude écologique de la zone méditerraéenne. Cañe bioclimatique de la zone méditerranéenne. Notice explicative. UNESCO. Paris.

Yanes, M., Suárez, F. and Manrique, J., 1991. La cogujada montesina, Galerida theklae, como depredador del caracol Otala lactea: com- portamiento alimenticio y selección de presa. Ardeola, 38: 297-303.

Yom-Tov, Y., 1971. Annual fluctuations in the water contení of desert snails. Malacological Review, 4: 121-126.

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Iberus, 26 (1): 53-63, 2008

Notes on the genus Anadema H. and A. Adams, 1854 (Gastropoda: Colloniidae)

Notas sobre el género Anadema H. y A. Adams, 1854 (Gastropoda: Colloniidae)

James H. MCLEAN* and Serge GOFAS**

Recibido el 15-1-2008. Aceptado el 23-IV-2008

ABSTRACT

Shell morphology and characters of the living animal of the poorly known, Atlantic Moroc- can species Anadema mocandrewii (Mórch, 1 864) are described and illustrated, based on beach collected specimens and a single live-collected specimen. The genus ¡s mono- typic and is assigned to the Colloniidae rather than Turbinidae because of the dome- shaped profile of the shell, open umbilicus, symmetrical tooth rows of the radula, lack of cephalic lappets, and the non-bicarinate ¡uvenile shell. Within the Colloniidae, it unusual for its relatively large mature shell, ¡uvenile shell with a keeled profile, and the lack of the secondary flap above the rachidian tooth. The species is regarded as sexually dimorphic, with the female shell having a raised periumbilical rim comparable to that of other tro- choideans modified for brooding by means of an enlarged umbilical cavity.

RESUMEN

Se describe e ilustra la morfología de la concha y del animal vivo de Anadema macan- drewii (Mórch, 1864), una especie poco conocida de la costa atlántica de Marruecos. El género es monotípico y se asigna a la familia Colloniidae, en lugar de a los Turbinidae por la forma abombada de la concha, el ombligo abierto, las filas de dientes radulares simétricas, la ausencia de lóbulos cefálicos y por su concha juvenil no bicarenada. Entre los Colloniidae, la especie es insólita por el tamaño relativamente grande de la concha adulta, el perfil de la concha juvenil con una quilla y la ausencia de un repliegue secun- dario sobre el diente raquídeo. Se considera que existe dimorfismo sexual en esta especie, pues la concha de la hembra tiene un reborde periumbilical elevado comparable con el de otros trocoideos modificados para incubar en una cavidad umbilical ampliada.

KEY WORDS: Trochoidea, Morocco, brooding, endemism. PALABRAS CLAVE: Trochoidea, Marruecos, incubación, endemismo.

INTRODUCTION

The poorly known genus Anadema been regarded as a trochid, a liotiid, a

H. and A. Adams, 1854 has at times colloniid, and a turbinid. Here we

* Natural History Museum of Los Angeles County, California 90007, USA.

** Departamento de Biología Animal, Facultad de Ciencias, Universidad de Málaga, E-29071 Málaga, Spain.

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Iberus , 26 (1), 2008

review the taxonomy and update what is now known about the type and only known species of this genus.

Anadema was proposed for the com- bination Omphalius (Anadema) caelata A. Adams, 1854, an Atlantic Moroccan species then thought to be a trochid in the absence of data on a calcified oper- culum. The species was not to be illus- trated until 19 years later but it was described in sufficient detail that its identity has never been in question. In his remarks that followed the Latin description of the species, Adams (1855: 39) wrote: "The character of this shell is so peculiar, on account of the internal spiral callus of the umbilicus, and the absence of characters which constitute allied forms, that I propose to consider it a subgenus of Omphalius , under the ñame of Anadema." The generic ñame Omphalius Philippi, 1847 now pertains to the Tegulinae, as defined by Hickman and McLean (1990).

Ten years after the introduction of Anadema , Mórch (1864: 46) reported that a living specimen had been col- lected at the type locality. Morch stated that: "Omphalius (Anadema) caelata is provided with a calcareous operculum, which proves that this species may be removed to Turbo. As there is already a T. caelata, L., I propose for this species Turbo macandrewii." Morch's placement of the species in Turbo predated most work on the genera of turbiniform gas- tropods, and was based on the assump- tion that any turbiniform species with a calcareous operculum could only be a Turbo. This was unfair to Arthur Adams, but the ICZN rules about secondary homonymy forcé us to abandon the original ñame and to use the replace- ment ñame. This ñame honors the re- discoverer Robert McAndrew, who dredged a living specimen at Mogador (now Essaouira), the type locality of the species.

The first shell figure known to us was provided still later by P. Fischer (1873), who used the replacement ñame Turbo macandrewii; this is a drawing that has been copied by many subsequent authors. The operculum has never been

figured and the repository of the oper- culate specimen examined by Morch is unknown.

Pilsbry (1888) ignored the replace- ment ñame and called it Leptothyra caelata, a not unreasonable choice, as it hardly resembles a species of Turbo. Lep- tothyra is now assigned to Colloniidae.

Wenz (1938: 340) recognized the genus Anadema and placed it in the turbinid subfamily Liotiinae, under a broad definition in which he also included genera with calcareous oper- cula related to Homalopoma.

Keen (1960: 270) placed Anadema in the more restricted Homalopomatinae, a group with fully calcified operculum, now subsumed under the turbinid sub- family Colloniinae in the classification of Hickman and McLean (1990).

Nordseick (1968: 33) overlooked Mórch (1864) and placed it in Liotiinae: "Deckel spiralig und mit Kalkbesatz, nicht verdickt", apparently having assumed that it must have the opercular definition of the now understood Lioti- idae, in which the operculum is multi- spiral with calcareous beads on the outer surface.

Resolution of the uncertainty is here provided by a preserved immature specimen with operculum, which was collected by the second author in 1991 at Essaouira (formerly Mogador), the type locality. We therefore take this opportu- nity to illustrate the species and confirm its placement.

MATERIALS

This report is based on material col- lected by the second author, which is now in the malacology collection of the Muséum National d'Histoire Naturelle, Paris (MNHN). The external features of the single live-collected specimen were drawn with the animal fully extended. Subsequent preservation of the speci- men resulted in retraction within the shell. It was later critical-point dried for SEM examination, after which it was rehydrated for extraction of the radula for SEM analysis.

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McLean AND GOFAS: Notes on the genus Anadema H. and A. Adams, 1854

SYSTEM ATICS

Superfamily Trochoidea Rafinesque, 1815

Hickman and McLean (1990) divided the family Turbinidae into a number of subfamilies, including Lioti- inae, Colloniinae, and Turbininae. However, Williams and Ozawa (2007) have reported that their data toward a molecular phylogeny of the family Turbinidae indicates that there are two well-supported groups within the previ- ously defined Turbinidae, which there- fore preeludes the placement of all of the subfamilies in the same family. In view of the ongoing reconsideration of the relationships among these groups.

we here treat the Liotiidae, Colloniidae, and Turbinidae at the family level within the superfamily Trochoidea, which simply raises the ranking in the existing classification. This has already been adopted by McLean and Kiel (2007). Additionally, and without dis- cussion, Warén and Bouchet in Bouchet and Rocroi (2005: 245) have separated Turbinoidea and Trochoidea at the superfamily level, which also indicates that the higher classification for trochi- form vetigastropods is currently unset- tled.

Family Colloniidae Cossmann, 1916 Subfamily Colloniinae Cossmann, 1916

Hickman and McLean (1990) pro- vided an extensive treatment of the Col- loniidae (then as Colloniinae), distin- guishing them from Turbinidae (then as Turbininae) on their smaller size, non-bi- carinate juvenile shell, lack of cephalic lappets, symmetrical tooth rows and inner lateral teeth that are not greatly enlarged. This is in contrast with the Turbinidae, characterized by larger size, bicarinate ju- venile shell, asymmetrical tooth rows and enlarged inner lateral teeth of the radula.

McLean and Kiel (2007) distin- guished two subfamilies within the Col-

loniidae, based on opercular morphol- ogy: the basal and mostly extinct Petropomatinae Cox in Knight et al., 1960, having a calcified operculum that is conical on the inner surface, with a fully multispiral pattern, and the Col- loniinae, in which the operculum is fíat on the inner surface with a multispiral pattern that changes to broadly pau- cispiral on the final volution. There is one living genus ( Liotipoma McLean and Kiel, 2007) of Petropomatinae, whereas there are numerous living and fossil genera of Colloniinae.

Genus Anadema H. and A. Adams, 1854

Anadema H. and A. Adams, 1854: 430 [as subgenus of Omphalius Philippi, 1847]. Type species (monotypy): Omphalius ( Anadema ) caelata A. Adams in H. and A. Adams, 1854 [= Turbo macan- drewii Morch, 1864; not Turbo caelata Linnaeus, 1758].

Anadema macandrewii (Morch, 1864) (Figs. 1-23)

Omphalius (Anadema) caelata A. Adams, in H and A. Adams, 1854: 430 [as type of new subgenus]. A. Adams, 1855: 39 [more detailed description].

Turbo macandrewii Morch, 1864: 46 [new ñame for secondary homonym Omphalius (Anadema) caelata, not Turbo caelata Linnaeus, 1758].

Turbo macandrewi. Fischer, 1873: 98, pl. 29, fig. 3 [first illustration]. Pasteur-Humbert, 1962: 132 [listed].

Leptothyra coelata [sic]. Pilsbry, 1888: 255, pl. 48, fig. 38 [figure after Fischer],

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Iberus, 26 (1), 2008

Turbo (Anadema) macandrewi. Pallary, 1920: 63.

Anadema coelata [sic]. Wenz, 1938: 340, fig. 795 [figure after Fischer]. Nordesick, 1968: 33, fig. 17.00

Anadema caelata. Keen, 1960: 270 [no figure]. Trew, 1992: 19 [listing of species described by H.& A. Adams].

Material examined: BMNH, 2 syntypes, BMNH 1968183, Mogador (now Essaouira), Atlantic Morocco (height 12.3 mm, diameter 16.6 mm; height 12.1 mm, diameter 17.3 mm). MNHN, Essaouira (formerly Mogador), Atlantic Morocco (31° 31' N, 9o 47' W), 1 live-collected male specimen and several beach-worn shells, leg. Gofas, 23 September 1991. MNHN, El Jadida, Atlantic Morocco (33° 16' N, 8o 29' W), beach worn shells, leg. Gofas, 26 September, 1991. MNHN, Mohammedia (for- merly Fedala), Atlantic Morocco (33° 43' N, 7o 21' W), 10 beach-worn shells, leg. Gofas, 1970-71.

Description : Because the genus is monotypic, the description that follows applies both to the genus and species.

Shell composed of 5 whorls with a low spire; profile dome-shaped, broader than high, suture not impressed; whorls weakly rounded, periphery of immature shell strongly projecting, forming a keel; periph- ery spinose in early stages, but losing spination at maturity; mature shell with a subangulate base; axial sculpture of fine, raised lamellae; spiral sculpture of low, strongly beaded cords; cords between suture and beaded basal cord increasing from three in juvenile to 6 at maturity; base slightly convex, basal cords of com- parable strength and beading to those of body whorl, increasing from three in juve- nile to 8 at maturity; spiral sculpture of both body whorl and base separated by narro w interspaces; axial lamellae well

developed in interspaces but not expressed on surface of nodular beads; umbilicus open in juvenile shell, closed in male shell at basal diameter of 9 mm; remaining open in female shell; umbilicus of mature female shell bordered by raised, unbeaded peripheral cord that partially obstructs final quarter whorl and connects directly at base of aperture; aperture oblique, thickened within, descending slightly on final whorl; interior nacreous, inner wall of aperture of female shell smooth, edge with U-shaped sinus; shell colour brick-red.

Shell dimensions. Mature female shell (Figs. 1-3): height 13.0, diameter 17.1 mm; immature male shell (Figs. 4- 6): height 4.9, diameter 9.1 mm; máximum dimensions possible for male shell unknown; immature female shell (Figs. 7-9), height 5.9, diameter 9.1 mm.

(Right page) Figures 1-15. Anadema macandrewii (Morch, 1864). 1-3: Mature, beach-worn female shell, from Essaouira, Morocco (MNHN), 3 views, height 13.0 mm, diameter 17.1 mm; 4-6: live- collected, immature male specimen with operculum in place, same locality (MNHN), 3 views, height 4.9 mm, diameter 9.1 mm; 7-9: immature, beach-worn female shell, from Mohammedia, Morocco (MNHN), 3 views, height 5.9 mm, diameter 9.1 mm; 10, 11: juvenile beach-worn shell, from Essaouira, Morocco (MNHN), 2 views, height 2.1 mm, diameter 5.0 mm; 12,13: juvenile shell with protoconch showing in umbilical view, from Essaouira, Morocco (MNHN), 2 views, diameter 2.7 mm; 14, 15: operculum of specimen shown in Figures 4-6 and 16, exterior and inte- rior views, máximum diameter 2.1 mm.

(Página derecha) Figuras 1-15. Anadema macandrewii (Morch, 1864). 1-3: Concha adulta, explayada, de una hembra, de Essaouira, Marruecos (MNHN), 3 vistas, altura 13,0 mm, diámetro 17,1 mm; 4-6: ejemplar macho inmaduro, recolectado vivo, con el opérculo cerrando la concha; misma localidad (MNHN), 3 vistas, altura 4,9 mm, diámetro 9,1 mm; 7-9: concha inmadura, explayada, de una hembra, de Mohammedia, Marruecos (MNHN), 3 vistas, altura 5,9 mm, diámetro 9,1 mm; 10, 11: concha juvenil explayada, de Essaouira, Marruecos (MNHN), 2 vistas, altura 2,1 mm, diámetro 5,0 mm; 12, 13: concha juvenil con la protoconcha visible desde el ombligo, de Essaouira, Marruecos (MNHN), 2 vistas, diámetro 2,7 mm; 14, 15: opérculo del ejemplar representado en las Figuras 4-6 y 16, vistas exterior e interior, diámetro máximo 2,1 mm.

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McLean AND GOFAS: Notes on the genus Anadema H. and A. Adams, 1854

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Iberus , 26 (1), 2008

Figure 16. Anadema macandrewii (Morch, 1864). Drawing of living specimen shown in Figures 4-6. Figura 16. Anadema macandrewii (Morch , 1864). Dibujo del animal vivo, del mismo ejemplar de las Figuras 4-6.

Juvenile shell (Figs. 10-13) not with raised axial lamellae, of low profile, exposing protoconch and early whorls in basal view; profile not equally bicari- nate, the upper carination spinose and more strongly projecting than lower, non-spinose carination; protoconch and first teleoconch whorl positioned slightly below level of second whorl.

Operculum (Figs. 14-15) calcareous, thick, with a concavity at the base where the white outer surface is coloured light reddish-brown. There is a strong ridge and groove of similar width leading to

the upper part, which bears strong pus- tules in the región adj acent to the col- umella; outer edge with a narrow groove; inner surface becoming broadly paucispiral in final volution. This oper- culum is chipped or somehow reduced at its inner edge, to the extent that the outline is not oval; the chitinous layer of the inner surface that shows at the lower left of Figure 15 is missing at the upper left.

Flead-foot (Figs. 16-19). Head pro- portionally large, provided anteriorly with a snout terminating in a broad.

(Right page) Figures 17-23. Anadema macandrewii (Morch, 1864). 17-19. Scanning electrón micrographs of critical-point dried specimen, same as shown in Figure 16. 17: general view of head-foot; 18: close-up of snout; note the absence of cephalic lappets; 19: close-up of right ante- rior bundle of epipodial tentacle. 20-23. Scanning electrón micrographs of the radula, same speci- men as Figure 16. 20: complete radula; 21: close-up of several complete rows; 22: detail of central and lateral teeth; 23: detail of marginal teeth. Abbreviations, ct: cephalic tentacle; et: epipodial tentacles; f: foot (pointing to propodium); sn: snout.

(Página derecha) Figuras 17-23. Anadema macandrewii (Morch, 1864). 17-19. Micrografías elec- trónicas de barrido del ejemplar de la Figura 16 deshidratado por punto crítico. 17: vista general de la cabeza y del pie; 18: vista aumentada del hocico; nótese la ausencia de lóbulos cefálicos; 19: vista aumentada de un haz anterior derecho de tentáculos epipodiales. 20-23. Micrografías electrónicas de barrido de la rádula, ejemplar de la Figura 16. 20: radula completa; 21: vista aumentada de algunas filas completas; 22: detalle de los dientes centrales y laterales; 23: detalle de los dientes marginales. Abre- viaturas, ct: tentáculo cefálico; et: tentáculos epipodiales; f: pie (señalado el propodio); sn: hocico.

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McLean AND GOFAS: Notes on the genus Anadema H. and A. Adams, 1854

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Iberusy 26 (1), 2008

flattened area surrounding the mouth, laterally with two prominent, smooth bulges containing rather large, black eyes and, next to these on the anterior side, two slender, villose cephalic tenta- cles; cephalic lappets lacking. Neck tobes present, rather symmetrical, undi- vided. Foot rather small, less than half the diametre of the shell when extended; each side of the epipodium provided in its anterior part with a cluster of three tentacles, the foremost on hardly more than a rounded bulge, the next two tapering and villose, hardly one-tenth of the cephalic tenta- cles in size; in the posterior part with two more tentacles similar in size and shape to the latter.

Radula (Figs. 20-23) strikingly sym- metrical, with broad rachidian having lateral extensions, and moderately long, tapered overhanging cusps; with four pairs of similar lateral teeth, which are elbowed like the rachidian and extend above the shaft of the next tooth; shaft of fifth lateral tooth not in cióse contact with shaft of fourth lateral tooth; this tooth broad on both sides, with a less prominent cusp than those of the inner lateral teeth or any of the marginal teeth; innermost pair of marginal teeth with short overhanging cusps, followed by four pairs of marginal teeth with longer cusps; outer marginal teeth with longer shafts, overhanging cusps shorter and deeply serrate on sides of the cusps.

The live-collected specimen (Figs. 4- 6, 16) reported here (diameter 9.1 mm) has a nearly closed umbilicus and a gen- erally unmodified base, with no indica- tion of the incipient formation of the

DISCUSSION

Knowledge of the genus Anadema has been slow to develop because the species A. macandrewii lives in the sublit- toral zone on rocky bottoms exposed to strong surf, where there have appar- ently been few efforts at collecting by diving due to the exposure, low visibil- ity, and extensive muddy bottoms off- shore in relatively shallow water. The

projecting rim of mature female shells; it is therefore identified as a male speci- men. There are immature beach-worn shells of about 10 mm in diameter (Figs. 7-9), which are considered to be female shells, having the beginning of a project- ing rim that will form the strong peri- umbilical angulation of the large female shell (Fig. 2). It is evident that male shells are much less frequent among the beach-worn shells. Because the male shell with an operculum is larger than any of the comparable beach-worn shells considered to be male shells, and because the lip is immature, there is no indication from the material at hand as to the possible size reached by male shells. It may be that male shells can reach a size similar to that of female shells. If so, they would differ from female shells in having a rounded umbilical wall, rather than the project- ing umbilical rim of female shells.

Both male and female shells seal the umbilicus upon attaining a half-grown diameter of about 10 mm. The female shell then proceeds to form a secondary umbilicus for the brooding cavity. The initial sealing of the umbilicus may help to protect the shell from exposure due to erosión of the apical whorls, which is also avoided in most marine gastropods by shell deposition of a plug from within.

There is variation in the peripheral spination of immature stages. The spination of the live-collected male specimen (Figs. 4-6) is stronger than that of any of the beach-worn shells of similar size, whether identified as male or female.

single live-collected specimen reported here from the intertidal zone is an unusual record for the species.

Systematic position: There is now no doubt that Anadema should be assigned to the family Colloniidae, on the basis of shell and opercular characters, charac- ters of the external anatomy, and the radula. The fine lamellar sculpture had

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McLean AND GOFAS: Notes on the genus Anadema H. and A. Adams, 1854

brought to mind a comparison with Liotiidae, but that is ruled out by the calcareous operculum.

There are many possibilities for opercular morphology in the Colloni- idae, just as there are in the Turbinidae (see Vermeij and Williams, 2007). There is no comparative work on the colloniid operculum, but the operculum of Anadema is within the range of possi- ble expression for the family. Immature shells of the Mediterranean turbinid species Bolma rugosa (Linnaeus, 1767) have a resemblance to Anadema macan- drewii in having a somewhat similar operculum and a spinose peripheral car- ination, but mature specimens of Bolma are much larger, have a higher profile and an impressed suture, a closed umbilicus and an expansive columellar callus that forms a columellar shield nearly as broad as the aperture. For a review of Bolma , see Beu and Ponder (1979). Anadema macandrewii differs from all illustrated species of Bolma in its low, dome-shaped profile and open umbili- cus at maturity.

The keeled early juvenile shells indi- cate that early sculpture is not evenly bicarinate, which is a defining feature for Turbinidae, according to the restricted definition provided by Hickman and McLean (1990: 55) at the previously recognized subfamily level. Most colloniids have the juvenile shell with even spiral cords, but there are exceptions to that generalization. The keeled early stage brings to mind the recently described Liotipoma McLean and Kiel, 2007, in the basal subfamily Petropomatinae, which also has an early keel.

The lack of cephalic lappets is consis- tent with the assignment to Colloniidae, in which lappets are lacking (Hickman and McLean, 1990). This is in contrast to the Turbinidae, in which the lappets are well-developed (Hickman and McLean, 1990), albeit they are small in the Mediterranean Bolma rugosa.

The radular morphology of Anadema provides convincing evidence that it is colloniid rather than turbinid because the tooth rows are perfectly symmetri-

cal, and the inner margináis are not greatly enlarged. In turbinids, the asym- metrical tooth row causes the tooth alignment to be skewed, because the large inner laterals must altérnate in zipper fashion when the radula is longi- tudinally folded (as detailed by Hickman and McLean, 1990).

Anadema is highly unusual within Colloniidae for its large size and its keeled early stage. With its máximum shell diameter of 17 mm, it may well be the largest known colloniid. All of the colloniid radulae illustrated by Hickman and McLean (1990) have a secondary flap that projects above the rachidian tooth; the radula of Anadema is unusual in not having the secondary flap. In addition, the morphology of the fifth lateral of Anadema seems also to be unusual for the family.

Larval brooding: Brooding of larvae within the umbilical cavity has been broadly reported among the Trochoidea (Hickman, 1992: 254). In the Trochidae it is known in Margantes vorticiferus, as shown by Lindberg and Doberteen (1981). In Liotiidae, it has been reported for Arene socorroensis by Shasky (1968) and again by Hertz (1998), and for "Munditia" subquadrata it has been reported by Burn (1976). In the Colloni- idae, it is known in the recently described genus Liotipoma, as reported by McLean and Kiel (2007). Its occur- rence in Anadema is therefore the second known example. In each of these cases, the umbilical rim of the female shell is raised to increase the volume of the umbilical cavity. Such a modification can be the only explanation for the strongly raised umbilical rim of what we interpret as the female shells of Anadema macandrewii.

The size reached by the shells of males remains to be discovered; it is possible that mature male shells are smaller than female shells. In support of that possibility, the operculum illus- trated here shows the expansión of the final volution that is characteristic of a mature operculum. However, this shell is somewhat immature because the final lip is not thickened. All beach-worn

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male shells in the material on hand seem to be immature. The immature male shells are represented by fewer specimens than the larger shells attrib- uted to, for reasons unknown.

ACKNOWLEDGMENTS

We thank Philippe Bouchet and Vir-

ginie Heros of the MNHN for arranging

the loan of the Anadema specimens.

Illustrations of shells (from photos by

BIBLIOGRAPHY

Adams, H., and Adams, A., 1854. Genera of Re- cent Mollusca, vol. 1. London, John Van Voorst, 484 pp.

Adams, A., 1855. Further contributions towards the natural history of the Trochi- dae; with a description of a new genus, and of several new species, from the Cumingian Collection. Proceedings of the Zoological Society of London, for 1854: 37-41, pl. 27.

Bellon-Humbert, C., 1974 ("1973")- Les Mol- lusques marins testacés du Maroc. Catalogue non critique. Premier supplément. Travaux de l'Institut Scientifique Chérifien, serie Zoologique, 37, 1-144, 23. pls.

Beu, A. G., and Ponder, W. F., 1979. A revisión of the species of Bolma Risso, 1826 (Gas- tropoda: Turbinidae). Records ofthe Australian Museum, 32 (1): 1-68.

Bouchet, P., and Rocroi, J. P., 2005. Classifi- cation and Nomenclátor of gastropod fami- lies. Malacologia, 47 (1-2): 1-397.

Burn, R., 1976. Shell with a built-in nest. Aus- tralian Shell News, 16: 3.

Fischer, P., 1873. Genre Turbo. Species General et Iconographie des Coquilles Vivantes [L. C. Kiener, continué par P. Fischer]. 128 pp., pls. 1-42.

Hertz, C. M., 1998. Arene socorroensis (Strong, 1934) with nestling nepionic larvae. The Fes- tivus, 30 (5): 65.

Hickman, C. S., 1992. Reproduction and de- velopment of trochacean gastropods. The Veliger, 35 (4): 245-272.

Hickman, C. S. and McLean, J. H., 1990. Sys- tematic revisión and suprageneric classifi- cation of trochacean gastropods. Natural His- tory Museum ofLos Angeles County, Science Se- ries, 35: 1-169.

the first author) were prepared in Photo- shop by Michelle Schwengel (formerly LACM) and píate preparation for the shells was completed by Ángel Valdés (formerly LACM). Critical-point dried preparation of the live-collected speci- men and the SEM views of the head- foot, as well as the SEM illustrations of the radula, were provided by Daniel L. Geiger of the Santa Barbara Museum of Natural FFistory. We thank the reviewers for their suggestions, which led to improvements in the paper.

Keen, A. M., 1960. [Recent Archaeogastropoda]. In Knight, J. B., L. R. Cox, A. M. Keen, R. L. Batten, E. L. Yochelson, and R. Robertson. 1960. Systematic descriptions (Archaeogas- tropoda). In Moore, R. C. (Ed.): Treatise on Invertebrate Paleontology, Part I, Mollusca 1, pp. 169-310, Geological Society of America and University of Kansas Press.

Lindberg, D. R. and Doberteen, R. A., 1981. Umbilical brood protection and sexual di- morphism in the boreal Pacific trochid gas- tropod, Margantes vorticiferus Dalí. Interna- tional Journal of Invertebrate Reproduction, 3: 347-355.

Mórch, O. A. L., 1864. Notes on shells. Amer- ican Journal of Conchology , 4: 46.

McLean, J. H. and Kiel, S., 2007. Cretaceous and living Colloniidae of the redefined sub- family Petropomatinae, with two new gen- era and one new species, with notes on op- ercular evolution in turbinoideans, and the fossil record of Liotiidae (Vetigastropoda: Turbinoidea). Palaontologische Zeitschrift, 81 (3): 254-266.

Nordsieck, F., 1968. Die europaischen Meeres- Gehduseschnecken (Prosobranchia) von Eismeer bis Kapverden und Mittelmeer. Gustav Fischer Verlag, Stuttgart, 273 pp.

Pallary, P., 1920. Exploration scientifique du Maroc organisée par la Société de Géographie de París et continuée par la Société des Sciences Na- turelles du Maroc. Deuxiéme fascicule. Mala- cologie (1912). Larose, Rabat and París, 108 p., 1 pl., 1 map.

Pasteur-Humbert, C., 1962. Les mollusques marine testacés du Maroc. Catalogue non critique. I. Les Gasteropodes. Travaux de ITn- stitut Scientifique Chérifien, serie Zoologie, 23: 1-245.

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McLean AND GOFAS: Notes on the genus Anadema H. and A. Adams, 1854

Pilsbry, H. A., 1888. Phasianellinae, Turbinidae, Delphinulinae. Manual of Conchology, vol. 10, 323 pp., 69 pls. [Neritidae, Adeorbiidae, Cy- clostrematidae, Liotiidae in this vol. by George W. Tryon, Jr.]

Shasky, D., 1969. Observations on Rósenla nido- rum (Pilsbry) and Arene socorroensis (Strong). The American Malacological Union, Annual Report for 1967: 74.

Trew, A., 1992. Henry and Arthur Adams's new molluscan ñames. National Museum of Wales, Cardiff, 63 pp.

Vermeij, G. J., and Williams, S. T., 2007. Pre- dation and the geography of opercular thick- ness in turbinid gastropods. Journal of Mol- luscan Studies, 73: 67-73.

Wenz, W., 1938. Gastropoda. Handbuch der Palao- zoologie, vol. 6. Teil 1: Allgemeiner Teil und Prosobranchia, Berlin, 1639 pp.

Williams, S. T. and Ozawa, T., 2006. Molecu- lar phylogeny suggests polyphyly of both the turban shells (family Turbinidae) and the superfamily Trochoidea (Mollusca: Veti- gastropoda). Molecular Phylogenetics and Evo- lution, 39: 33-51.

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A new species of Mangelia (Turridae: Mangeliinae) from the Mediterranean Sea

Una nueva especie de Mangelia (Turridae: Mangeliinae) del Mediterráneo

Charles CACHIA* and Constantine MIFSUD**

Recibido el 17-VII-2007. Aceptado el 12-III-2008

ABSTRACT

A new species Mangelia melitensis nov. sp., from Malta, is introduced and compared with other similar congeneric species.

RESUMEN

Se describe una nueva especie Mangelia melitensis, de Malta, y se compara con especies congenéricas de aspecto similar.

KEY WORDS: Mollusca, Conoidea, Turridae, Mangeliinae, Mangelia nov. sp., Mediterranean. PALABRAS CLAVE: Mollusca, Conoidea, Turridae, Mangeliinae, Mangelia nov. sp., Mediterráneo.

INTRODUCTION

The genus Mangelia is represented in the Mediterranean Sea by about 28 species (CLEMAM 2007). The shells are slender, fusiform in shape, with a sculp- ture consisting of axial, and often spiral sculpture. The siphonal canal is short and open and the columella is smooth without any processes. The mollusc has a wide foot, long tentacles with eyes sit- uated on the sides of the stalks and at about 2/ 3 their height, a long siphon and the body is mostly of a transparent white colouration, but sometimes with opaque coloured streaks or blotches, especially on the siphon. The radula consists of hollow marginal teeth, rarely barbed, with an irregular basal swelling (McLean, 1971). The animal lacks an operculum. The diet consists mainly of

* 1, Alley 1, St. Catherine Street, Qormi QRM, Malta

** 5, Triq ir-Rghajja, Rabat RBT 2486, Malta

polychaete worms, sometimes larger than the mollusc itself. (C. M. pers. obs.)

Certain authors (Bouquoy, Dautzenberg and Dollfus, 1883; Powell, 1966; van Aartsen and Fehr de Wal, 1978) have proposed that the Mediterranean species classification should be separated into two genera, Mangelia (Risso, 1826) type species Man- gelia attenuata (Montagu, 1803) and Mangiliella (B.D.D., 1826) type species Mangiliella multilineolata (Deshayes, 1836). The proposition is based on the type of development of the protoconch. Mangelia has a multi-spiral or plank- totrophic type of protoconch, usually consisting of 2 l/i or more whorls while Mangiliella has a paucispiral or direct type of protoconch consisting of 1 1 /lio

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Iberus, 26 (1), 2008

2 whorls. Although this arrangement is very convenient for separating the species, Bouchet (1990) advised against such methods for creating genera and subgenera in this already problematic family.

The Mediterranean species have been dealt with by several authors (Nordsieck, 1977; van Aartsen and Fehr de Wal, 1978; Sabelli, Giannuzzi-

-Savelli and Bedulli, 1990; Cachia, Mifsud and Sammut, 2001; Gruppo Malacologico Livornese and Gruppo Malacologica Romagnolo, 2005).

During our ongoing research on the marine mollusca which inhabit the coasts of the Maltese Islands, we have come across many specimens of a dis- tinct Mangelia species which is new to Science. It will be introduced herein.

SYSTEMATICS

Superfamily Conoidea Vaught, 1989 Family Turridae Swainson, 1840 Subfamily Mangeliinae Vaught, 1989 Genus Mangelia Risso, 1826

Mangelia melitensis nov. sp. (Figs. 1, 2)

Material studied: All studied material is from the Maltese Islands. Holotvpe. collection number BMNH 20070312 (H= 6mm, W= 2.5mm), and two paratypes, collection number BMNH 20070313, off Gnejna Bay, in sand and algae from 40 m., x-2006, The Natural History Museum, London. Three paratypes, off Ras il-Wahx, 35 m., ix-1992, collection number MNHN 9988, Muséum National d'Histoire Naturelle, París. Three paratypes, off Rdum id-Delli, 50 m., ix-2006, collection number. TAU MO 57001, National Collections of Natural History, Department of Zoology, Tel Aviv University. Four paratypes, off Ras il-Wahx, 25-30 m., ix-1992, and three paratypes, St Thomas Bay, 3-4 m., viii-1987, National Museum of Natural History (Mdina, Malta). Other Paratypes: Salina Bay, 4 m viii-2000, 21 shells; off Rdum id-Delli, 60 m, viii-2006, 5 shells; off Cirkewwa Point, 34 m, viii-1996, 14 shells, in prívate collection of Charles Cachia. [Coll. No 1185]. Off St. Paul's Bay, 40-50 m., ix-1986, 3 shells; Qammieh, Cumnija, 50 m., viii-1986, 4 shells; St. Thomas Bay, 3-4 m., viii-1987, 11 shells; Bahar ic-Caghaq, beached, i-1991, 5 shells; Gozo Island, Dwejra, Coral cave, in sand, 25 m., 1 shell, 9-vi-2001 (leg. Anthony Sammut); off Golden Bay, 40 m, iii-1991, 9 shells; off Ras il-Wahx, 25-30 m., ix-1992, 31 shells off Rdum id- Delli, 50 m., ix-2006, 9 shells, in prívate collection of Constantine Mifsud [coll. No. M1601]. Off Ras il-Wahx, 25-30 m., ix-1992, 2 shells, in prívate collection of Charles Sammut. Salina Bay, 4 m., viii-1998, 2 shells (C. Cachia leg.), in prívate collection of Gert Lindner.

Type locality: Gnejna Bay, Maltese Islands.

Etymology: Named after the type locality.

Description : Shell small, rather fragüe, fusiform, typical of the genus. Proto- conch consists of 2 1 ¡i, rounded, trans- parent white, glassy whorls, the last with a few small, close-set axial riblets crossed by spiral micro-striae. Teleoconch con- sists of up to four whorls which are sub- angulated at their adapical third and curving regularly towards the suture.

Sculpture of 8-9 narrow, flexuous, slight- ly opisthocline, axial ribs which continué to the base. Their interspaces are about twice as wide. The whole surface of the

shell is covered with dense micro-spiral striae of about the same thickness and close-set axial growth lines, producing an iridescent pattern. There are about 45- 50 of these micro-spiral striae at the penultimate whorl. There are also 5-6 well spaced, thicker spiral chords at the base of the shell, near the siphonal canal. Aperture about half height of shell. Out- er lip sharp, thin and fragüe, thickened internally, with its topmost part clearly curved. Lip varix present in some speci- mens. Sinus shallow. Columella smooth.

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Cachia AND MlFSUD: A new species of Mangelia from the Mediterranean Sea

Figure 1. Mangelia melitensis nov. sp., shells. A: holotype from off Gnejna Bay, in sand and algae, 40 m (height 6 mm); B: paratype from the type locality (height 6 mm); C, D: paratype from off Ras il-Wahx, 25-30 m (height 6.1 mm).

Figura 1. Mangelia melitensis nov. sp., conchas. A: holotipo, frente a Gnejna Bay, en arena y algas, 40 m (altura 6 mm); B: paratipo de la localidad tipo (altura 6 mm); C, D: paratipo, frente a Ras il—Wahx, 25-30 m (altura 6,1 mm).

Siphonal canal short and wide. The shell colour is white or beige. Rarely, some specimens are decorated with four, faint, brownish spiral bands or with tiny, brown sub-sutural blotches on the penultimate whorl, while others have a dark blotch at the middle of the exterior of the outer lip. A single specimen is completely brown.

DISCUSSION

M. melitensis nov. sp. had already been introduced as Mangelia sp. A. in Cachia et al. (2001). It differs from all the other Mediterranean forms of the M. unifasciata (Deshayes, 1835) complex, to which it is very similar, by the lack of bold spiral cords on its whorls. It is similar in this respect to M. costulata Risso, 1826 [= M. smithii (Forbes, 1840)], but in that species the spiral striae are fewer, flatter, much bolder, and continuous, not crossed by growth lines, while their interspaces are deeply incised. Mangelia costulata never forms a thickened rib on the

The animal is transparent white with large black eyes at about two-thirds of the height of the tentacle stems. The foot has opaque white spots, while the siphon has small opaque yellowish spots. There is no operculum.

The species is found near or in Posi- donia oceánica (Linnaeus) Delile, substra- tum at depths of 3 to 50 metres.

aperture, unlike the present species: Moreover, in M. costulata the last proto- conch whorl has a bold reticulate type of sculpture, whilst in M. melitensis nov. sp. this whorl has only close-set flex- uous axials with spiral micro-striae. M. costulata usually has a continuous wide brown band on the ultimate whorl and the animal has a bright orange spotted siphon.

Mangelia melitensis nov. sp., also offers similarities to Mangelia costata (Donovan, 1804). In that species however the whorls are very evenly convex not somewhat subangulated as

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Figure 2. Mangelia melitensis nov. sp., scanning electrón micrographs, same paratype as Figures 1C-D. A: protoconch; B: detail of the sculpture on a spire whorl.

Figure 2. Mangelia melitensis nov. sp., vistas en microscopía electrónica, mismo paratipo que las Figura 1 C-D. A: protoconcha; B: detalle de la escultura en una vuelta de la espira.

in Mangelia melitensis nov. sp. The shell is also smaller, rather glossy, differently coloured, of a more fusiform aspect and with a slightly different protoconch. The animal is completely white.

Distribution: The Maltese Islands. The authors have not come across any specimens of M. melitensis nov. sp. from any other Mediterranean locality.

BIBLIOGRAPHY

Buquoy, E., Dautzenberg, P. and Dollfus, G., 1882-1886. Les Mollusques marins du Rous- sillon. I: Gastropodes. París, Bailliére, 570 pp. Bouchet, P., 1990. Turrid genera and mode of development: The use and abuse of proto- conch morphology. Malacologia, 32 (1): 69-77. Cachia, C., Mifsud, C. and Sammut, P., 2001. The Marine Mollusca of the Maltese Islands, Part 3 Neogastropoda, Backhuys Publishers, 266 pp.. Leiden.

CLEMAM, Unitas Malacologica; Checklist of European Marine Mollusca: Web Page: http: / / www.somali.asso.fr /clemam/bio- taxis.php [accessed 5-vi-2007]

Gruppo Malacologico Livornese and Gruppo Malacologico Romagnolo, 2005. Nota sulle Mangelia Mediterranee. Notiziario S.I.M., 23 (9-12): 22-33.

MacLean, J. H., 1971. A revised classification of the Family Turridae, with the proposal of new Subfamilies, genera and subgenera from the eastem Pacific. The Veliger, 14 (1): 114-130.

ACKNOWLEDGEMENTS

We would like to thank our colleague P. Sammut (Rabat, Malta) for revising the manuscript and G. Lindner (Germany) for his kind disposition. The scanning elec- trón micrographs for this paper were pro- duced at the University of Málaga with the help of Gregorio Martín Caballero.

Mifsud, C., 1998. The molluscan species living in Maltese Posidonia meadows. La Conchiglia, 30 (287): 37-48, 61.

Nordsieck, F., 1977. Turridae of the European Seas. "La Pirámide" for La Conchiglia, 131 pp. Rome.

Nordsieck, F., 1982. Die europaischen Meeres- Gehauseschnecken. 2nd edition. 539 pp. Gus- tav Fischer, Stuttgart

Powell, A. W. B. 1966. The Molluscan families Speightiidae and Turridae. Bulletin of the Auckland Institute and Museum, 5, 184 pp. + 23 plates. New Zealand.

Sabelli, B., Gianuzzi-Savelli, R. and Bedulli, D., 1990. Catalogo annotato dei molluschi marini del Mediterráneo, S. I. M. Librería Nat- uralística Bolognese, Vol. 1. xiv, 1-348. Bologna.

van Aarsten, J. J. and Fehr de Wahl, M.C., 1978. The sub family Mangeliinae Fischer, 1887 in the Mediterranean. Conchiglie, 14 (3- 6): 97-110.

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Iberas , 26 (1): 69-80, 2008

Catálogo de los bivalvos marinos del sector central del Golfo de Valencia (España)

Checklist of the marine bivalves in the central sector of the Gulf of Valencia (Spain)

Jorge C. TAMAYO GOYA*

Recibido el 12-11-2007. Aceptado el 31-III-2008

RESUMEN

Se presenta una lista con 1 84 especies de Bivalvos marinos citados en la literatura y rea> lectados por el autor entre 1998 y 2008, en la costa del Golfo de Valencia, sector cen- tral: 39° 42' N, 0o 12' W (Playa de Canet de Berenguer, Sagunto) - 38° 55' N, 0o 03# W (Playa de Oliva), Mediterráneo occidental. Cari fervensis se cita por primera vez en ¡a zona y se confirma la existencia de poblaciones establecidas de Eastonia rugosa, Fulvia fragilis y Lentidium mediterraneum.

ABSTRACT

A list is presented with 1 84 species of marine Bivalves cited in the literature or collected by the author between 1 998 and 2007, along the coast of Gulf of Valencia, central sec- tor: 39° 42' N, 0o 12' W (Playa de Canet de Berenguer, Sagunto) - 38° 55' N, 0o 03' W (Playa de Oliva), Western Mediterranean. Gari fervensis is cited for the first time in the area and the occurrence of established populations is confirmed for Eastonia rugosa, Ful- via fragilis and Lentidium mediterraneum.

PALABRAS CLAVE: Catálogo, moluscos, bivalvos, Golfo de Valencia, Mar Mediterráneo. KEY WORDS: Checklist, molluscs, bivalves, Gulf of Valencia, Mediterranean Sea.

INTRODUCCIÓN

En este trabajo se presenta una actua- lización de la lista faunística de moluscos bivalvos de la Bahía de Valencia. Estos complementan un catálogo reciente- mente publicado (Oliver Baldoví, 2007) donde se aporta una actualización de Gasterópodos marinos testáceos de la zona sur del Golfo de Valencia.

La gran mayoría de las conchas reco- lectadas son explayadas, por lo que no se puede indicar su hábitat originario. En mucha menor medida, se han obtenido

buceando a pulmón-con tubo (entre -2 y -3 m) o recogidas por una embarcación "marisquera" faenando a escasos metros de la costa (zona infralitoral). Las recogi- das de muestras se han ido realizando a lo largo de todas las estaciones entre los años 1998 y 2008 y no se ha seguido una metodología concreta.

Los sustratos sedimentarios que constituyen el hábitat de las comunida- des presentes en el piso infralitoral son, las correspondientes a: arenas finas

* C/Polo y Peyrolón, 37, izda 16, 46201, Valencia.

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Figura 1 . Localidades de muestreo en el Golfo de Valencia. Figure 1. Sampling sites in Gulf of Valencia.

superficiales, arenas finas bien calibra- das (entre -2/ -3 m. y -20/ -25 m.), arenas finas fangosas (entre -20/-25 m. y -35/- 40 m.), arenas con proporciones peque- ñas de finos (<15%) (consideradas como transición entre ambos sustratos) y los fondos detríticos.

El sustrato rocoso está presente en mucha menor medida, lo mismo que las praderas de Posidonia oceánica (en mucha mayor proporción de mata muerta que degradada, y que suele extenderse en una distribución batimé- trica entre -5 m y -20 m), así como la Cymodocea nodosa y la Caulerpa prolifera. Las arenas gruesas y gravillas, ocupan franjas a profundidades variables y sujetas a corrientes marinas.

A continuación en profundidad, en la plataforma continental, está el piso circalitoral (entre -40 m. y -100 m.), de escasa pendiente, en el que están pre- sentes los fondos detríticos costeros. Los fondos fangosos terrígenos (a partir de - 100/-150 m.) se extienden por zonas muy amplias del fondo marino.

El litoral en estudio, eminentemente sedimentario, se caracteriza por la suce- sión casi continuada de playas de arena fina, sólo interrumpidas por las instala- ciones portuarias, las desembocaduras fluviales (áreas de fondos fangosos) y el Cabo de Cullera (acantilado mediano)

Las poblaciones en cuyas playas se han efectuado la recogida de ejemplares son colindantes entre sí y han sido agru- padas, de norte a sur, en las siguientes subzonas (Fig. 1), siendo la B y la D en donde mayor número de muéstreos se han realizado:

A: (Canet d'En Berenguer), Sagunto, Puzol y El Puig. Predominan las arenas finas bien calibradas, en mucha menor medida las de arenas finas fangosas y las extensiones de mata muerta de Posi- donia. El puerto de Sagunto y el puerto deportivo de Canet de Berenguer, la planta siderúrgica de Sagunto, el emisa- rio de Canet de Berenguer, y la desem- bocadura del río Palancia, son agentes determinantes en la configuración sedi- mentaria de esta zona del litoral.

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Tamayo GOYA: Catálogo de los bivalvos marinos del sector central del Golfo de Valencia

B: Puebla de Farnals, Massamagrell, Meliana, Alboraya y las playas al norte de Valencia. Las arenas finas fangosas predominan sobre las arenas finas bien calibradas. Es de mencionar el sustrato rocoso frente al Puerto de Valencia y las extensiones de mata muerta de Posidonia, en mayor superficie que las de la subzona A. Él puerto deportivo de Port sa Playa, el Barranco de Carraixet y el emisario de Vera (al norte del Puerto de Valencia), son los agentes de esta subzona.

C: Playas al sur de Valencia. Hay mucho mayor predominio de las arenas finas bien calibradas sobre las arenas finas fangosas. El Puerto de Valencia, la desembocadura del río Turia, el emisa- rio del sur del Puerto y las Golas del Pujol y de El Perellonet (provenientes de La Albufera), son los agentes a destacar.

D: Sueca y Cullera . Es la subzona con mayor proporción de arenas finas bien calibradas y con menor de finas fangosas en el área de estudio. A reseñar también, la presencia de mata muerta de Posidonia en el afloramiento rocoso frente a Cullera. Cabe mencionar en esta subzona, la desembocadura del Jucar y las Golas de El Perelló y la del Estany.

E: Tavernes de la Valldigna, Xeraco, Xeresa, Gandía, Daimuz, Guardamar, Miramar, Piles y Oliva. Las arenas finas fangosas predominan sobre las finas bien calibradas. Frente a Gandía existe otro enclave rocoso con presencia de Posidonia. Los puertos de Gandía y Oliva, constituyen lo más destacable como agentes determinantes.

SISTEMÁTICA

En la Tabla I se presenta el listado de especies encontradas en el área de estudio, junto con el número de especí- menes encontrados, sus sectores de dis- tribución y citas bibliográficas. Esta lista ha sido ordenada de acuerdo con la cla- sificación propuesta por CLEMAM. Check List of European Marine Mollusca: chttp:// www.somali-

asso.fr/ demarro .

DISCUSIÓN

Glycymeris violacescens (Lamarck, 1819)

Es una especie muy presente en gran parte del litoral de Valencia que con fre- cuencia se muestra con un polimorfismo y policromía muy característicos (Fig. 2), predominando el contorno de la concha menos subcuadrangular, muchas veces más oblicua; el color gris negruzco- azulado, principalmente en la mitad superior y umbo, combinado con los colores tierra (beige y marrón) y con mucha mayor superficie de mancha en el interior de la valva; generalmente, los umbos más separados y con mayor área cardinal; cohabitando en proporciones similares con los ejemplares más comunes-tipo, más frecuentemente divulgados (Fig. 3).

Fulviafragilis (Forsskal in Niehbur, 1775)

Se confirma (Fig. 4) la presencia en la zona de esta especie, previamente citada en Cullera por Zenetos et al. (2004) a partir de ejemplares recolectados en 1991. Ello indica que esta especie está formando poblaciones perennes en la zona, al igual que sucede en otras partes del Mediterráneo (Crocetta, 2005; Vardala-Theodorou , 1999).

Eastonia rugosa (Helbling, 1779)

Especie presente ocasionalmente en este sector del Golfo de Valencia, salvo en la subzona B en la que si es habitual hallarla. En la playa de Meliana (subzona B) es donde se concentra la gran mayoría de los individuos de esta especie encon- trados en esta zona del litoral (Fig. 5). Decenas y decenas de conchas de indivi- duos jóvenes y adultos son depositadas todos los años en esta playa. En esta subzona B, también se localiza una impor- tante concentración de ejemplares, aunque en menor medida, de Lutraria magna (da Costa, 1778) y Venericardia antiquata (Linné, 1758). Es de notar que esta especie mani- fiesta una tendencia a ampliar su exten- sión en el Mediterráneo, siendo reciente- mente observada en abundancia en las costas italianas en localidades donde no se conocía anteriormente (La Valle, Vani, Liboni y Smriglio, 2007).

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Tabla I. Listado de especies encontradas en el área de estudio. Ej: concha recolectada explayada; Ej*: entre 1 y 3 ejemplares recolectados; Ej*: entre 1 y 3 ejemplares recolectados, deteriorados; L: especie presente en la colección de referencia del laboratorio de Biología Marina de la Universidad de Valencia (1982-1989, García Carrascosa, no publicado) o citada en la bibliografía reseñada, sin ejemplar recolectado por el autor. Las letras (ABCDE) corresponden a los sectores de la Figura 1 en los que se han recolectado ejemplares. Las referencias a las citas se indican como sigue: (1) Colección de referencia del laboratorio de la Universidad de Valencia; (2) ApáRICI SEGUER, Rowland, Taylor y García Carrascosa, 1996; (3) Bonnin y Rodríguez Babio, 1990; (4) Costa, García Carrascosa, Monzó, Peris, Stubing y Valero, 1984; (3) Generalitat Valenciana, Conselleria de Agricultura y Medio Ambiente, 1994-1997; (6) Giner Ponce, 1989; (7) Hidalgo, 1917; (8) Montero Agüera, 1971; (9) Ramón Herrero, 1993; (10) ROSELLÓ, 1910; (11) SÁNCHEZ Diana, 1980. Los nombres subrayados corresponden a las especies que están comentadas en este trabajo.

Tal? le I. List of the species found in the studied urea. Ej: shell collected on the beach; Ej*: 1 to 3 speci- mens found; Ej*: 1 to 3 specimens found, damaged; L: species found in the reference collection deposited in the Marine Biology laboratory ofthe University of Valencia (1982-1989, García Carrascosa, unpu- blished data) or cited in literature, no specimens collected by the author. Letters (ABCDE) refer to Figure 1 sectors. Literature cited as follows: (1) reference collection deposited in the laboratory ofthe University of Valencia; (2) APARICI SEGUER, R.OWLAND, TAYLOR AND GARCIA CARRASCOSA, 1996;

(3) Bonnin y Rodríguez Babio, 1990; (4) Costa, García Carrascosa, Monzó, Peris, Stubing and Valero, 1984; (5) Generalitat Valenciana, Conselleria de Agricultura y Medio Ambiente, 1994-1997; (6) Giner Ponce, 1989; (7) Hidalgo, 1917; (8) Montero Agüera, 1971; (9) Ramón Herrero, 1993; (10) Roselló, 1910; (11) Sánchez Diana, 1980. Underlined ñames are discussed in this paper.

Especie	Especímenes	Localización	Referencias
Familia SOLEMYIDAE
Solemya fogata (Poli, 1791)	L		3, 7, 8,10,11
Familia NUCULIDAE
Nucula nitidosa Winckworth, 1 930	E¡	BCD	3, 5, 7, 8,10,11
Nucula nucleus (Linné, 1758)	E¡	ABD	1,3, 5, 6, 7, 8,10,11
Nucula sulcata Bronn, 1831	L		1,2, 3, 5, 6, 7, 8,11
Familia NUCULANIDAE
Nuculana pella (Linné, 1767)	E¡*	ABCDE	2, 3, 5, 6, 7, 8,10,11
Saccella commutata (Phiíippi, 1 844)	L		3, 5, 7, 8,10,11
Familia ARCIDAE
Arca noae Linné, 1758	E¡	ABCDE	2, 3, 5, 6, 7, 8,10,11
Arca Terragona Poli, 1795	L		U, 6, 7, 8,10,11
Barbada barbota (Linné, 1 7 58)	E¡	ABCDE	3, 8,10,11
Barbada clatbrata (Defrance, 1816)	L		3,
Anadara corbuloides (Monterosato, 1 880)	E¡*	B	3, 7, 8,10,11
Anadara polil (Mayer, 1 868)	E¡*	B	3, 7, 8,10,11
Bathyarca pectunculoides (Scacchi, 1 835)	L		3, 7, 8,11
Bathyarca phillppiana (Nyst, 1 848)	L		3,8
Familia NOETIIDAE
Striarca ladea (Linné, 1758)	E¡	ABCDE	1,2, 3, 5, 6, 7, 8,10,11
Familia GLYCYMERIDAE
Glycymeris blmaculata (Poli, 1 795)	L		3, 5, 7, 8,10,11
Glycymeris glycymeris (Linné, 1758)	E¡*	D	U, 3, 4, 6, 7,10,11
Glycymeris violascescens (Lamarck, 1819)	E¡	ABCDE	1,3, 5, 6, 7, 8,10,11
Familia MYTILIDAE
Mytilus edulis Linné, 1758	E¡	ABCDE	3, 7, 8,10,11

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Tamayo Goya: Catálogo de los bivalvos marinos del sector central del Golfo de Valencia

Tabla I. Continuación. Table I. Continuation.

Especie	Especímenes	Localización	Referencias
Mytilus galloprovincialis Lamarck, 1819	E¡	ABCDE	1,2, 3, 4,5
Mytilaster minimus (Poli, 1795)	E¡*	D	1,3, 7, 8,10,11
Gregariella petagnae (Scacchi, 1 832)	E¡	DE	1,2, 3, 8,10,11
Musculus costalatus (Risso, 1 826)	E¡	B	1,3, 6, 7, 8,10,11
Musculus subpictus (Cantraire, 1 835)	Ej*	B	1,2, 3, 8,10,11
Lithophaga lithophago (Linné, 1758)	Ei	ABCDE	1,3, 4, 5, 6, 7, 8,10,11
Myoforceps aristatus (Dillwyn, 1 81 7)	L		3, 7, 8,10,11
Modiolus adriaticus (Lamarck, 1819)	E¡	BD	3,5, 7, 8,10,11
Modiolus mortorelli (Hidalgo, 1 878)	L		3, 4, 7, 8,10,11
Modiolus barbatus (Linné, 1 7 58)	E¡	ABCDE	U, 5, 6, 7, 8,10,11
Amygdalum agglutinans (Cantraine, 1 835)	El	D	5
Modiolula phaseolino (Phillipi, 1 844)	L		3, 7, 8,10,11
Familia PINNIDAE
Pinna nobilis Linné, 1758	L		3, 4, 7, 8,10,11
Pinna rudis Linné, 1758	L		3, 8,11
Atrina pectinata (Linné, 1 767)	E¡	CDE	3, 7,10,11
Familia PTERIIDAE
Pieria hirundo (Linné, 1758)	Ei	C	3, 4, 5, 7, 8,10, 11
Familia PECTINIDAE
Pecten ¡acobeus (Linné, 1 7 58)	Ei	ABDE	3, 4, 5, 7, 8,10,11
Pecten maximus (Linné, 1758)	L		3, 7, 8,11
Aequipecten opercularis (Linné, 1758)	Ei	DE	3, 5, 7, 8,10,11
íissopecten byalinus (Poli, 1 795)	Ei	ACD	3, 7, 8,10,11
Palliolum incomparable (Risso, 1 826)	L		3, 7, 8,10,11
Pseudamussium clavatum (Poli, 1795)	L		3, 7, 8,10,11
Hyalopecten similis (Laskey, 1811)	L		3, 7, 8,10
Propeamussium fenestratum (Forbes, 1 844)	L		3,
Chlamys flexuosa (Poli, 1 795)	Ei	BCD	3, 4, 7, 8,10,11
Cblamys glabra Linné, 1758)	Ei	BDE	3, 5, 7, 8,10,11
Chlamys pesfelis (Linné, 1 758)	Ei	BD	3, 7, 8,10,11
Cblamys multistrata (Poli, 1795)	Ei	BCDE	3, 5, 8,11
Cblamys varia (Linné, 1758)	Ei	ABCDE	3, 5, 6, 7, 8,10,11
Familia Spondylidae
Spondylus gaederopus Linné, 1 7 58	Ei	ABCD	3, 5, 7, 8,10,11
Familia ANOMIIDAE
Anomia ephippium Linné, 1 7 58	Ei	ABCDE	2, 3, 5, 7, 8,10,11
Pododesmus patelliformis (Linné, 1761)	L		3
Familia LIMIDAE
tima lima (Linné, 1758)	Ei	ABCD	1,3, 5, 6, 7, 8,10,11
timaria bians (Gmelin, 1791)	Ei	ABCDE	1,3, 4, 5, 6, 7, 8,10,11
limaría tuberculata Olivi, 1792	Ei	BCDE	1,3, 4, 6, 7, 8,10,11
Limea loscombii (Sowerby G.B., 1 824)	L		3, 4,5
[¡matulo subauriculata (Montagu, 1808)	L		3, 7, 8,10,11
Notolimea crassa (Forbes, 1 844)	L		3,
Familia OSTREIDAE
Ostrea edulis Linné, 1758