Present Status of the Endangered Limpet Cymbula Nigra (Gastropoda
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Animal Biodiversity and Conservation 34.2 (2011) 319 Present status of the endangered limpet Cymbula nigra (Gastropoda, Patellidae) in Ceuta: how do substrate heterogeneity and area accessibility affect population structure? G. A. Rivera–Ingraham, F. Espinosa & J. C. García–Gómez Rivera–Ingraham, G. A., Espinosa, F. & García–Gómez, J. C., 2011. Present status of the endangered limpet Cymbula nigra (Gastropoda, Patellidae) in Ceuta: how do substrate heterogeneity and area accessibility affect population structure? Animal Biodiversity and Conservation, 34.2: 319–330. Abstract Present status of the endangered limpet Cymbula nigra (Gastropoda, Patellidae) in Ceuta: how do substrate heterogeneity and area accessibility affect population structure?— Cymbula nigra (Gastropoda, Patellidae) is a threatened giant patellid limpet found on the North African coast from Namibia to Algeria. The objective of this study was to estimate the total number of individuals present in Ceuta (Strait of Gibraltar) and to determine the effect of certain physical parameters on population structure and abundance. Between 2006 and 2010 we conducted an exhaustive census in the area. Results indicate that Ceuta could be home to 48,473 individuals. The most important populations were recorded on the North Bay, characterized by its Atlantic influence. While for other similar species, such as Patella ferruginea, human accessibility to the area plays an important role in determining the structure of populations, we found that substrate roughness (small scale topographic heterogeneity) is the main determining factor in this species. Populations located on medium to low topographic heterogeneity substrates showed higher percentages of medium and large size individuals. However, recruitment rates did not differ between substrata of different roughness. Finally, and through the analysis of the C. nigra populations located on some recently constructed jetties, we obtained interesting new data regarding individual growth rates, thus contributing to our knowledge of the population structure of the species. Key words: Limpet, Endangered species, Cymbula nigra, Substrate heterogeneity, Strait of Gibraltar, Ceuta. Resumen Situación actual en Ceuta de la lapa Cymbula nigra (Gastropoda, Patellidae), una especie en peligro: ¿cómo afecta la heterogeneidad del substrato y la accesibilidad del área a la estructura de las poblaciones?— Cymbula nigra (Gastropoda, Patellidae) es una lapa gigante amenazada que se encuentra distribuida por las costas norteafricanas desde Namibia a Argelia. El objetivo del presente estudio era estimar el número total de individuos presentes en Ceuta (Estrecho de Gibraltar) y determinar el efecto de ciertos parámetros físicos sobre la abundancia y estructura de las poblaciones. Para conseguirlo, entre 2006 y 2010, se llevó a cabo un censo exhaustivo en la zona. Los resultados indicaron que Ceuta podría albergar unos 48.473 individuos. Las poblaciones más importantes fueron registradas en la Bahía del Norte de la ciudad, caracterizada por su influencia atlántica. Mientras que en otras espe- cies similares, como Patella ferruginea, la accesibilidad de la zona por parte del hombre juega un papel importante en la determinación de la abundancia y estructura de las poblaciones, nuestros resultados indicaron que en esta especie el principal factor determinante es la rugosidad del sustrato (heterogeneidad topográfica a pequeña escala). En este sentido, aquellas poblaciones localizadas sobre sustratos de media a baja complejidad mostraron may- ores porcentajes de individuos de tamaño mediano y grande. Sin embargo, las tasas de reclutamiento no variaron entre sustratos de diferente rugosidad. Finalmente, a través del análisis de poblaciones de C. nigra localizadas sobre algunos diques de construcción reciente, se obtuvieron nuevos e interesantes datos relacionados con tasas individuales de crecimiento, contribuyendo así al conocimiento de la estructura de poblaciones de esta especie. Palabras clave: Lapas, Especies amenazadas, Cymbula nigra, Heterogeneidad del sustrato, Estrecho de Gibraltar, Ceuta. (Received: 28 VI 11; Conditional acceptance: 10 XI 11; Final acceptance: 18 XI 11) Georgina Alexandra Rivera–Ingraham, Free Espinosa, José Carlos García–Gómez, Lab. de Biología Marina, Depto. de Fisiología y Zoología, Univ. de Sevilla, Av. Reina Mercedes 6, 41012, Sevilla, España (Spain). Corresponding author: G. A. Rivera–Ingraham. E–mail: [email protected] ISSN: 1578–665X © 2011 Museu de Ciències Naturals de Barcelona 320 Rivera–Ingraham et al. Introduction the date when these structures were finished allowed us to obtain average growth rates and compare these The commonly known Black limpet (Cymbula nigra) with previous data available for the species. (da Costa, 1771) (former Patella nigra) is the largest limpet in Europe, reaching up to 13.3 cm (Rivera–In- graham et al., 2011a). It is present in the southernmost Material and methods area of the Iberian peninsula, having been located in Algeciras (Guerra–García et al., 2006; Rivera–Ingra- Study site ham, 2010), Fuengirola (Spada & Maldonado Quiles, 1974; Grandfils & Vega, 1982; Christiaens, 1983), The present study was conducted in Ceuta, located Mijas (Martínez & Peñas, 1996) and, more recently, on the African coast of the Strait of Gibraltar (fig. 1A) . in Granada (Moreno & Arroyo, 2008). It has also This area is known to have large C. nigra populations been found at Alboran Island (Moreno, 2006; Peñas (Rivera–Ingraham, 2010). The coasts of this city are et al., 2006; Templado et al., 2006; Moreno & Arroyo, composed of natural rocky shores, beaches and islets. 2008), although its presence here is considered rare. There are also many breakwaters and jetties, and a Along the north African coast, the species occurs commercial port. from Namibia to Algeria (Koufopanou et al., 1999) and has large populations in Ceuta (Templado et al., 2004; Sampling methods Espinosa et al., 2007) and Melilla (Pasteur–Humbert, 1962). The coast of Senegal was thought to be the To estimate the total number of C. nigra individuals centre of the species’ dispersion (Christiaens, 1974) present in Ceuta we used the methodology described but more recent morphological and molecular studies in Rivera–Ingraham et al. (2011b).The complete suggest that the species might have originated on the coastline was divided into 14 sectors (see fig. 1B) south–western African coasts (Ridgway et al., 1998; and for each one, and only for rocky shores, a total Koufopanou et al., 1999; Templado et al., 2004). of 10 transects of 10 m were randomly established Cymbula nigra is currently catalogued as an 'en- on the coastline. These transects occupied the whole dangered or threatened species' by the Barcelona vertical distribution range of the species (intertidal Convention (Annex II, 1993), as 'strictly protected' areas and the upper sublitoral regions, up to 5 m by the Berne Convention (Annex II, 1995), and as depth). Surveys were always carried out during low 'vulnerable' by the Andalusian Red List of Threatened tide (tide amplitudes usually ranging from 0.41 to 1.01) Invertebrate Species (Moreno & Arroyo, 2008). It is and subtidal regions were sampled by diving. Each surprising therefore that little is known about the biol- C. nigra individual located in these transects was ogy and ecology of the species. Most of the recent measured to the nearest millimetre using a calliper literature that mentions C. nigra is related to phylo- as in Guerra–García et al. (2004), Espinosa (2009) genetic studies of the family Patellidae (Ridgway et or Rivera–Ingraham (2010). The number of individu- al., 1998; Koufopanou et al., 1999; Sá–Pinto et al., als present in these transects was extrapolated to 2005) or genetic aspects of the species (Espinosa et the total length of coastline in the sector, which was al., 2010; Nakano & Espinosa, 2010). Recent studies measured using 1:9,000 maps. For the specific case indicate that C. nigra recruits in the upper intertidal of islets, jetties and breakwaters, a complete census levels while the largest individuals occupy the lower was carried out when possible. The complete coastline intertidal areas (Rivera–Ingraham et al., 2011a) and was inspected from 2006 to 2010. Additionally, and can be found up to 5 m deep (Rivera–Ingraham, for each of the prospected locations, some physical 2010). It is a protandric hermaphrodite species that parameters were recorded and sectors were classi- reproduces mainly in late autumn but also, to a lesser fied based on: i) type of substrate (natural/artificial) extent, in spring (Frenkiel, 1975; Rivera–Ingraham, ii) accessibility by humans (high/medium/low) and 2010). Cymbula nigra is a territorial species, and iii) substrate roughness or small scale 'topographical individuals defend a well defined area from other heterogeneity index' (THI) (high/medium/low) (refer to macroorganisms (Rivera–Ingraham, 2010). Rivera–Ingraham et al. (2011b) for further details). It Despite the interest in quantifying populations of en- is also important to note that in the present study, dangered species (e.g. Paracuellos et al., 2003) this has individuals present in Ceuta are considered part of not been done to date for C. nigra. The present study a metapopulation composed of genetically connected describes the population of C. nigra from the coast of sub–populations (see review by Badii & Abreu, 2006). Ceuta, and estimates the total number of individuals. Moreover, and taking into account that C. nigra has Analyses been