Unexpected abundance and long-term relative stability of the brown alga Cystoseira amentacea, hitherto regarded as a threatened species, in the north-western Mediterranean Sea

Highlights

• Mapping of Cystoseira amentacea over 1832 km.

• Analysis of 467 historical records over more than 300 years.

• Presence along 1125 km of shoreline.

• No evidence of loss except in 4 locations.

• Absence or low abundance in the vicinity of ports and large sewage outfalls.

Abstract

Cystoseira amentacea is a Mediterranean endemic alga thriving on very shallow rocky substrates. It has been considered as a threatened species, having experienced a steady decline and is therefore protected by international conventions. The historical distribution of the species has been assessed along the French Mediterranean coast, on the basis of 467 articles and herbarium vouchers. We have produced an accurate map of its current distribution and abundance along 1832 km of coastline, through in situ surveys. C. amentacea was observed along 1125 km of shoreline, including 33% of almost continuous or continuous belt. In most of its range, there is no evidence of loss, except in 4 areas of Provence, French Riviera and Corsica. A significant relation was found between the absence or low abundance of C. amentacea and the vicinity of ports and large sewage outfalls. The status of conservation of the species should therefore be reassessed.

Introduction

The coastal ecosystems are highly impacted all over the world, due to the cumulative impact of increasing human pressure (e.g. destruction of habitats, pollution, species introduction, overfishing, coastal aquaculture and global warming). None of the forms of impact affecting the coastal ecosystems exists in isolation. Different pressures act over time and in unison, with a possible synergy effect, to affect the species, the ecosystems and their ability to deliver ecosystem services (e.g. Worm et al., 2006, Halpern et al., 2008, Waycott et al., 2009). The Mediterranean Sea is a hotspot of marine biodiversity that is under siege due to high demographic pressure, a high percentage of worldwide shipping and tourism and the highest rate of biological invasions (Bianchi and Morri, 2000, Galil, 2000, Boudouresque and Verlaque, 2002, Lotze et al., 2006, Coll et al., 2010, Lejeusne et al., 2010, Zenetos et al., 2010, UNEP/MAP, 2012, Bianchi et al., 2014).

Along the temperate rocky coasts, the large canopy-forming kelps (Laminariales, Phaeophyceae, Ochrophyta) and fucoids (Fucales, Phaeophyceae, Ochrophyta) represent the dominant species in pristine environment (Dayton, 1985, Steneck et al., 2002, Schiel and Foster, 2006). They provide shelter, food, habitat and nurseries to a multitude of species; they provide high primary production involved in the maintaining of diversified trophic levels; the largest species attenuate wave action (Steneck et al., 2002). These seaweeds can be controlled by a top-down mechanism mainly in the case of the sublittoral species, while the subsurface species are controlled by a bottom-up mechanism (Hereu et al., 2008, Cardona et al., 2013). The decline of kelps and fucoids is a worldwide phenomenon due, directly or indirectly, to human activities (Steneck et al., 2002, Díez et al., 2003, Helmuth et al., 2006, Worm and Lotze, 2006, Airoldi and Beck, 2007, Hawkins et al., 2008, Wernberg et al., 2010, Schiel, 2011, Lamela-Silvarrey et al., 2012, Raybaud et al., 2013, Filbee-Dexter and Scheibling, 2014). Some taxa, have been driven to regional extinction (Thibaut et al., 2005). These changes are leading to shifts in habitat structure from a state with canopy forming species to alternative states, in the worst cases to barren grounds composed of filamentous and encrusting species (Micheli et al., 2005, Perkol-Finkel and Airoldi, 2010, Sala et al., 2011, Sala et al., 2012, Parravicini et al., 2013, Filbee-Dexter and Scheibling, 2014).

In the Mediterranean Sea, species of the genus Cystoseira C. Agardh are habitat-forming species dominating several benthic assemblages from the littoral fringe down to the lower sublittoral zone (Feldmann, 1937, Molinier, 1960, Pignatti, 1962, Verlaque, 1987, Ballesteros, 1988, Ballesteros, 1990a, Ballesteros, 1990b, Giaccone et al., 1994). Their zonation is dependent on different environmental conditions (light, temperature, hydrodynamism and grazing) (Sauvageau, 1912, Ollivier, 1929, Vergés et al., 2009). Losses of fucoids have been reported all around the Mediterranean Sea caused by habitat destruction, eutrophication and overgrazing by herbivores leading to a shift to less structural complexity, such as turf-forming, filamentous or other ephemeral seaweeds or barrens grounds where urchin density is a driver of habitat homogenisation (Munda, 1974, Munda, 1982, Munda, 1993, Thibaut et al., 2005, Devescovi and Ivesa, 2007, Airoldi et al., 2008, Falace et al., 2010, Fraschetti et al., 2011, Giakoumi et al., 2012, Sala et al., 2012, Bianchi et al., 2014, Templado, 2014).

Seaweeds living in the rocky intertidal zone or in the sublittoral fringe can endure hard ecological conditions (desiccation, high variation of temperature, salinity and insolation, strong wave actions, etc.).

Among the 51 taxonomically accepted taxa of the genus Cystoseira (Guiry and Guiry, 2014), 36 are present in the Mediterranean Sea, 30 are endemic to the Mediterranean, and only 3 live exclusively in the Mediterranean littoral fringe (i.e. the upper level of the sublittoral, from the mean sea level down to less than 1 m depth): Cystoseira mediterranea Sauvageau in the western basin, Cystoseira tamarascifolia (Hudson) Papenfuss in the Alboran Sea and Cystoseira amentacea (C. Agardh) Bory de Saint-Vincent in all the Mediterranean; two poorly characterised varieties var. amentacea and var. stricta Montagne, are sometimes considered (Ribera et al., 1992, Cormaci et al., 2012, Guiry and Guiry, 2014) but they will not be distinguished here. Because of their shallow habitat, these species escape overgrazing by most of the large herbivores, e.g. the sea urchins Paracentrotus lividus (Lamarck 1816) and Arbacia lixula (Linnaeus 1758) and the teleost Sarpa salpa (Linnaeus 1758) unlike the others subtidal fucoids (Cormaci and Furnari, 1999, Thibaut et al., 2005, Serio et al., 2006, Vergés et al., 2009). All these sub-surface species are considered as vulnerable to sea surface pollution, habitat destruction, trampling and a number of regression events have been reported all around the Mediterranean Sea (Bellan-Santini, 1968b, Desrosiers et al., 1982, Desrosiers et al., 1986, Cecere et al., 1996, Rodriguez-Prieto and Polo, 1996, Cormaci et al., 2001, Soltan et al., 2001, Milazzo et al., 2002, Thibaut et al., 2005, Díez et al., 2009, Arévalo et al., 2007, Falace et al., 2010, Sales et al., 2011, Tsiamis et al., 2013). These taxa are also facing the low frequency natural disturbances called in Spanish ‘minva’ (very low tide for a long period of time, due to meteorological events), leading to mass mortality of the shallowest Cystoseira species (Huvé, 1970, Rodriguez-Prieto, 1992). In disturbed areas, Cystoseira species can be replaced by dense stands of fast growing Corallina spp. (Corallinales, Rhodophytes) and/or the mussel Mytilus galloprovincialis Lamarck, 1819 (Mytiloida, molluscs), which become dominant, forming extensive and wide belts along the shore (Berner, 1931, Bellan-Santini, 1964, Bellan-Santini, 1965, Bellan-Santini, 1968a, Bellan-Santini, 1968b, Huvé, 1970, Arnoux and Bellan-Santini, 1972, Bellan and Bellan-Santini, 1972, Astier, 1975, Augier, 1977, Fernandez and Niell, 1982, Desrosiers et al., 1982, Desrosiers et al., 1986, Thomas, 1983, Janssens et al., 1993, Soltan et al., 2001, Arévalo et al., 2007, Maggi et al., 2009, Falace et al., 2010). The interactions between Cystoseira species, turf-forming algae, herbivores and associated species have been extensively studied at different spatial and temporal scales and levels of protection (Benedetti-Cecchi and Cinelli, 1992a, Benedetti-Cecchi and Cinelli, 1992b, Benedetti-Cecchi and Cinelli, 1995, Menconi et al., 1999, Ruitton et al., 2000, Benedetti-Cecchi, 2001, Benedetti-Cecchi et al., 2001, Bulleri et al., 2002, Maggi et al., 2009, Maggi et al., 2012, Fraschetti et al., 2012, Tamburello et al., 2013). C. amentacea can also be replaced by the tolerant Cystoseira compressa (Esper) Gerloff and Nizamuddin (Mangialajo et al., 2012).

Along the whole of the French Mediterranean coasts, two species are restricted to the upper sublittoral zone, C. mediterranea in the western part along the French Catalonian coast (Sauvageau, 1912, Feldmann, 1937), and C. amentacea in Provence, French Riviera and Corsica. The latter taxon is widely distributed in the Mediterranean (Ribera et al., 1992). A non-Mediterranean record, from Sudan (East Africa) is regarded as a misidentification (Papenfuss, 1968). C. amentacea possesses a 40 cm high caespitose thallus and a basal holdfast a few centimetres wide. The species forms extensive stands on shallow rocky wave-exposed zones (Agardh, 1842, Molinier, 1960, Boudouresque, 1971a, Boudouresque, 1971b). As thalli are negatively buoyant and the maximum distance for egg dissemination is low (∼few dozen cm, Mangialajo et al., 2012), the species is suspected of having low dispersal ability. C. amentacea is one of the most productive Mediterranean seaweeds (Bellan-Santini, 1963, Bellan and Bellan-Santini, 1972, Susini, 2006), because of steady exposure to turbulence (frequent emersion/immersion), which maintains a high nutrient uptake (Epiard-Lahaye et al., 1987).

Because of its habitat preferences, C. amentacea has been considered as one of the species most severely impacted by coastal development and sewage outfalls (Bellan-Santini, 1964, Bellan-Santini, 1965, Bellan-Santini, 1966, Bellan-Santini, 1968b, Bellan and Pérès, 1970, Arnoux and Bellan-Santini, 1972, Bellan and Bellan-Santini, 1972, Astier, 1975, Belsher, 1977, Desrosiers et al., 1982, Desrosiers et al., 1986, Thomas, 1983, Janssens et al., 1993, Sinnassamy et al., 1993, Soltan et al., 2001, Bulleri et al., 2002, Falace et al., 2010). C. amentacea is also harvested for the cosmetics industry (Max Pellegrini, pers. comm.). Furthermore, the species is thought to be vulnerable to oil spills and chemical releases at the sea surface (Bellan-Santini, 1968b). The species is considered to have a high ecological status within the framework of the EU Water-Framework Directive (2000/60/EC) (Orfanidis et al., 2001, Panayotidis et al., 2004, Ballesteros et al., 2007, Mangialajo et al., 2008, Cecchi et al., 2009, Sfriso and Facca, 2011, Nikolic et al., 2013).

C. amentacea is currently listed as a species strictly protected under the Berne Convention (Annex I 1979), together with 4 other taxa (C. mediterranea, C. sedoides, C. spinosa, C. zosteroides); all the Mediterranean species of the genus Cystoseira, except C. compressa have been listed under Annex II of the Barcelona convention (2010). All the Mediterranean Cystoseira species are under surveillance by international organizations such as the IUCN, the RAC/ASP and MedPan. Like all the species of the genus Cystoseira, C. amentacea’s stands are an habitat and listed as Habitat of Community Interest by the UE (Micheli et al., 2013).

The use of historical data in marine ecology is growing, as they provide a baseline of animal and plant populations in very lightly disturbed areas so changes can be analysed over a long time period (Jackson et al., 2001, Thibaut et al., 2005, Sáenz-Arroyo et al., 2005, Barsanti et al., 2007, Babalis, 2011, Lotze et al., 2010, Montefalcone et al., 2013, Husa et al., 2014). Most studies of habitat loss or coastal urbanisation, however, focus only on local scales and short periods over contemporary times. Whilst this focus is also necessary, the preoccupation with these local and present-day drivers means that we are often not aware of the past extension of the species and of the regional context of local studies.

In order to analyse the long-term changes in C. amentacea populations along the French Mediterranean coasts, we collected all available data (herbarium vouchers, published and grey literature) and we have compared them to our field surveys. Because most of the data collected over the last centuries are qualitative, the aim of this study was: (i) to give a present exhaustive quantitative map of the distribution of C. amentacea along the French Mediterranean coasts, including Corsica; (ii) to compare the present distribution with historical data; (iii) and to highlight the eventual sites of regression and identify the possible causes.