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Variation and Ontogenetic Changes of Opercular Paleae in a Population Of SCIENTIA MARINA 79(1) March 2015, 137-150, Barcelona (Spain) ISSN-L: 0214-8358 doi: http://dx.doi.org/10.3989/scimar.04127.19A Variation and ontogenetic changes of opercular paleae in a population of Sabellaria spinulosa (Polychaeta: Sabellaridae) from the South Adriatic Sea, with remarks on larval development Marco Lezzi 1, Frine Cardone 2, Barbara Mikac 3, Adriana Giangrande 1 1 DiSTeBA University of Salento, CoNISMa, Via Provinciale Lecce- Monteroni, 73100 Lecce, Italy. E-mail: [email protected] 2 Department of Zoology, Via Orabona 4, 70125 University of Bari, Italy. 3 Center for Marine Research, Ruđer Boković Institute, Giordano Paliaga 5, 52210 Rovinj, Croatia. Summary: Sabellaria alcocki Gravier, 1906, described for the Indian Ocean, should not be present in the Mediterranean area. Though S. spinulosa alcocki, a Mediterranean variety, can be well-distinguished from S. alcocki, it has recently been referred to as S. alcocki. Thus, S. alcocki appears in the Italian coast checklist. The recent finding of S. spinulosa reefs along the southern Adriatic coast, the first report of these biogenic constructions in the Mediterranean area, allowed us to compare its morphological variability with that of S. alcocki. A morphometric analysis of the opercular paleae showed a great deal of intrapopulation, size-independent variation, which cannot justify the existence of varieties within S. spinulosa. Moreover, the analysis of post-settlement development showed that opercular features change during individual growth. Recently set- tled individuals resemble S. alcocki, while the more advanced life stages become closer to S. spinulosa. Accordingly, we hypothesize that part of the erroneous Mediterranean records of S. alcocki could correspond to specimens of S. spinulosa at different stages of development. Keywords: Annelida; Sabellariidae; Mediterranean; Adriatic; morphometry; development. Variación y cambios ontogenéticos de paleae opercular en una población de Sabellaria spinulosa (Polychaeta: Sabel- laridae) desde el mar Adriático del sur, con comentarios sobre el desarrollo larvario Resumen: Sabellaria alcocki Gravier, 1906, descrita en el Océano Índico, no debería estar presente en el Mediterráneo. A pesar de que S. spinulosa alcocki, una variedad mediterránea, es fácilmente diferenciable de S. alcocki, esta especie ha sido recientemente citada como S. alcocki. Como consecuencia, esta última aparece en la lista faunística de las costas italianas. El reciente hallazgo de arrecifes de S. spinulosa en el sur del Adriático, la primera cita de estas formaciones biogénicas en el Mediterráneo, ha permitido comparar su variabilidad morfológica con la de S. alcocki. El análisis morfométrico de las carac- terísticas de las paleas operculares mostró una gran variabilidad intrapoblacional, independiente de la talla, lo cual no justifica la existencia de variedades en S. spinulosa. Por otro lado, el análisis del desarrollo post-asentamiento mostró que las carac- terísticas operculares cambian con el crecimiento individual. Los individuos recién asentados son más similares a S. alcocki, mientras que se asemejan más a S. spinulosa en etapas posteriores. Así pues se sugiere que una parte de los registros erróneos de S. alcocki en el Mediterráneo podrían corresponder a especímenes de S. spinulosa en diferentes etapas de desarrollo. Palabras clave: Annelida; Sabellariidae; Mediterráneo; Adriático; morfometría; desarrollo. Citation/Como citar este artículo: Lezzi M., Cardone F., Mikac B., Giangrande A. 2015. Variation and ontogenetic changes of opercular paleae in a population of Sabellaria spinulosa (Polychaeta: Sabellaridae) from the South Adriatic Sea, with remarks on larval development. Sci. Mar. 79(1): 137-150. doi: http://dx.doi.org/10.3989/scimar.04127.19A Editor: D. Martin. Received: July 16, 2014. Accepted: February 11, 2015. Published: February 23, 2015. Copyright: © 2015 CSIC. This is an open-access article distributed under the Creative Commons Attribution-Non Com- mercial Lisence (by-nc) Spain 3.0. INTRODUCTION Nishi et al. 2010, Hutchings et al. 2012). As in all the sabellariid genera, the anterior part of the body shows The genus Sabellaria (Annelida, Sabellariidae) a truncated surface forming an operculum used to seal includes at least 39 species worldwide (Kirtley 1994, the tube entrance to avoid desiccation and predation, 138 • M. Lezzi et al. and as a tool in shaping and arranging sand grains dur- on each side. Sabellaria spinulosa and S. alcocki are ing tube construction (Eckelbarger 1975). Opercular also distinguished by the absence of nuchal spines in features are of paramount taxonomic importance in the latter (Kirtley 1994). Sabellariidae, but their taxonomy and phylogeny are Although S. alcocki has been considered as exclu- not yet solved (Capa et al. 2012). sive of the Indian Ocean (Nishi et al. 2010, Hutch- In Sabellaria, the operculum consists of three rows ings et al. 2012) and has not been reported in the of chaetae called paleae. An outer row formed during Mediterranean Sea (Coll et al. 2010), the species was ontogenesis by the pair of outer chaetigerous sacs, and included in the checklist of the Italian coast (Castelli middle and inner rows formed by inner chaetigerous et al. 2008) and continues to be reported in Mediter- sacs (Eckelbarger 1975). Opercular paleae can be high- ranean faunistic papers (Parapar et al. 1992, Çinar et ly variable in form and size, and their morphology is of al. 2006, 2008). As a consequence, the geographical particular interest in systematics because of the relative distribution of S. spinulosa and S. alcocki remains uniformity of other structures. However, the opercular unclear (Read 2014). This is probably due to the paleae may show ontogenetic changes, with the “inter- above-mentioned high morphological variability of mediate” forms of paleae differing from those of adult S. spinulosa. Fauvel (1914) considered S. alcocki as worms (Kirtley 1994). Moreover, the paleae can break one of the varieties of S. spinulosa summarized in and be altered by epifaunal growths and abrasion, in- Fauvel (1927). Accordingly, S. spinulosa var. alcocki creasing their morphological variability. differs from S. spinulosa in having the middle oper- Three species of Sabellaria are currently known for cular paleae with alternating long and short falciform the Mediterranean Sea: S. alveolata (Linnaeus, 1767), blades. However, no mention of nuchal spines (“soies S. spinulosa (Leuckart, 1849), and S. alcocki Gravier, aciculaires” sensu Fauvel 1927) is present in Fauvel’s 1906 (Castelli et al. 2008). Sabellaria alveolata forms description of S. spinulosa var. alcocki. Following extensive long-lasting (4 to 9 years) intertidal biogenic Fauvel (1927), “S. spinulosa alcocki” has been report- reefs along most Atlantic European coasts (Wilson ed worldwide (e.g. Kirtley 1994, Fauchald and Bel- 1971, Achary 1974, Gruet 1982, 1986). Along the Ital- lan 2013). More recently, however, S. alcocki started ian coast, S. alveolata reefs occur in the Ligurian and again to be reported as a separate species, leading to the Tyrrhenian Sea (Dubois et al. 2002, La Porta and several erroneous reports around the world (e.g. Hart- Nicoletti 2009). man 1944, Achary 1974, Fauchald 1977), including Sabellaria spinulosa and S. alcocki are smaller the Mediterranean coast (Parapar et al. 1992, Castelli than S. alveolata and inhabit the subtidal and lower et al. 2008, Çinar et al. 2006, 2008). intertidal/sublittoral fringes. Sabellaria spinulosa has Within the framework of a multidisciplinary project been described from the North Sea (Leuckart 1849) on the functional and ecological role of marine biocon- and S. alcocki from the Indian Ocean (Gravier 1906). structions, large biogenic formations of S. spinulosa In Mediterranean areas, S. spinulosa occurs solitary were found along the Adriatic coast, offering an op- or forming small clumps (Wilson 1970). By contrast, portunity to examine the opercular variability of this dense aggregations forming reefs up to 60 cm high and species. In the present paper, we report the analyses extending over several hectares can be found in areas of this variability in adults, coupled with a labora- with very high levels of suspended sediment in the tory study on larval development to describe changes North Sea (Wilson 1970, 1971) and around the British during the opercular formation. As mentioned above, Isles (Pearce et al. 2011). Reefs may persist for many the opercular paleae undergo ontogenetic changes in years, although individual clumps may be regularly shape (Eckelbarger 1975). Also, during the develop- formed and disintegrated (Jones et al. 2000). In fact, ment of S. spinulosa, the “primary paleae” are lost and sabellarian reef structure and morphology are mainly replaced by “secondary paleae” progressively resem- influenced by currents, among other environmental bling the outer opercular paleae of the adult (Wilson conditions, with cyclical phases of construction and 1929, 1970). Such a loss and progressive formation of destruction (Gruet 1982, 1986, Porras et al. 1996, Dau- the opercular paleae in post-settlement stages has only vin 1997, Dubois et al. 2002). been reported for S. vulgaris Verril, 1873, although the Sabellaria spinulosa seems to be a fast growing an- size required to reach the stage having the adult paleae nual form, which is able to quickly recolonize areas was not defined. lost due to winter storms. Many thin crust-like struc- Taking into account that the development
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