Annual growth and environmental relationships of the invasive species Sargassum muticum and Undaria pinnatifida in the lagoon of Venice
Introduction
Over the past two decades, the Mediterranean Sea has been colonized by several non-indigenous macroalgae with most species coming from the Indo-Pacific area (Verlaque, 1994, Verlaque, 2001, Boudouresque and Verlaque, 2002, Occhipinti-Ambrogi, 2002, Cormaci et al., 2004, Zenetos et al., 2010, Occhipinti et al., 2011). Many new species were introduced via the Suez Canal or via the Straits of Gibraltar. Such species first colonized warm areas and, later, spread to other regions due to recent temperature increases (Raitsos Dionysios et al., 2010). Three main factors contributed to the species introduction and spreading: 1) heavy tourist and commercial naval traffic with extra-Mediterranean countries; 2) the import of shellfish products and 3) aquaculture (Zenetos et al., 2012). Areas along the Italian coasts, the northern Adriatic lagoons, the Mar Piccolo of Taranto and some major ports are at risk of colonization by several non-indigenous species (NIS) due to intense and frequent international trades above all with the Indo-Pacific countries. The Venice Lagoon, in particular, has high tourist and commercial naval activities. From 2005 to 2011, 4142–5032 ships reached the port of Venice each year (Anonimous, 2010) and 500 additional ships reached the port of Chioggia. Most of the ships unballasted in the port areas. Also, in the Venice Lagoon ca. 3000 ha are used to farm bivalve mollusks with a present annual production of 10–15 ktonnes; in the same basin there are several decontamination plants and two big wholesale fish markets: Chioggia and Venice. In 2010 such markets had a business volume of 46 and 57 million euros, respectively, which represented the 60% of the whole Northern Adriatic activity (VERITAS, 2011). Most of the shellfish products sold in markets came from extra-Mediterranean countries. Due to such activities, in the Venice Lagoon, every year new species are recorded (Occhipinti-Ambrogi, 2000), mainly macroalgae (Sfriso et al., 2009, Sfriso et al., 2012). More recently Zenetos et al. (2010) produced a total list of 125 alien macrophytes for the Mediterranean Sea. Out of those 49 have been recorded in the Adriatic Sea and 33 are present in the Lagoon of Venice.
Six species are considered invasive or potentially invasive: i.e. Codium fragile subsp. fragile (Suringar) Hariot, Gracilaria vermiculophylla (Ohmi) Papenfuss, Grateloupia turuturu Yamada, Heterosiphonia japonica Yendo, Sargassum muticum (Yendo) Fensholt and Undaria pinnatifida (Harvey) Suringar. Codium, Grateloupia and Heterosiphonia are benthic taxa, present in many areas of the lagoon, but with a negligible biomass. Gracilaria vermiculophylla is the most recent introduction (Sfriso et al., 2010, Sfriso et al., 2012). It usually grows free-floating from spring to autumn, becoming invasive and reaching high biomasses in eutrophic and turbid environments, where it can replace natives, including Ulvaceae.
Sargassum muticum and Undaria pinnatifida, are the most abundant invasive species that colonize the hard substrata of the historical centre of Venice, Chioggia and many islands (Curiel and Marzocchi, 2010). U. pinnatifida is a cold-temperate species originating from China, Japan and Korea. S. muticum is a temperate species distributed along a large native latitudinal range (from cold to warm waters) (Zenetos et al., 2010). They were firstly recorded during the early 1990s near the wholesale fishing markets of Chioggia and the Venice historical centre (Gargiulo et al., 1992, Rismondo et al., 1993) and rapidly spread into a large part of the basin (Curiel et al., 1998, Curiel and Marzocchi, 2010). These invasive species need hard substrata to develop and do not grow in floating form. Both species are strongly attached to the substratum by means of fibrous disks (Sargassum) or thick rhizoids (Undaria) that make eradication difficult and very expensive. U. pinnatifida presents cyclical alternation between macroscopic sporophytes and microscopic gametophytic stages. After the winter-spring growth the large and long sporophytes disappear completely in summer. S. muticum is a perennial species only represented by the sporophyte: the gametophytic stage is restricted to the gametangia differentiated in the conceptacles. The perennial part of individual (holdfast and axis) subsist during the resting period. Both species do not compete with the species covering soft substrata such as Ulvaceae, Gracilariaceae and other NIS, i.e. Gracilaria vermiculophylla and Solieria filiformis, which preferentially grow unattached to the substratum and produce most of the lagoon algal biomass.
Since the last decade, in April–May, Sargassum muticum and Undari pinnatifida have reached such a density (up to 15–20 kg m−2, Curiel and Marzocchi, 2010) and size (up to 8 m and 2 m in length, respectively, Sfriso et al., 2009) that their presence has created a public concern. After detachment from the canals and the port banks, where they form thick belts (10–25 kg fwt m−2), the large and long thalli, especially Sargassum, hinder the small navigation. Luckily these species cannot grow further after detachment and are usually moved into the sea by tidal exchange or get stranded along island and the mainland shores.
Moreover, their local use for animal or human food or the production of alginates or other compounds is negligible due to their high pollutant content. In fact, the historical centre of Venice is devoid of depuration plants and sewages, after decantation, flow directly into the canals. Undaria shows a significant accumulation of inorganic (metals and metalloids, Caliceti et al., 2002) and organic (PAHs, PCBs, pesticides, Pavoni et al., 2003) pollutants. There is no information for Sargassum in Venice Lagoon but its surficial exposure with primary laterals floating on the water surface and the fact that it is a perennial species surely favor its contamination, especially by PAHs and petroleum compounds which are usually spread on the water surface.
In addition to pollutant accumulation, until now the studies of Sargassum and Undaria in Venice Lagoon dealt with biomass, spatial and temporal distribution and impact on the native species (Curiel et al., 1998, Curiel and Marzocchi, 2010). No information on their seasonal growth and relationship with environmental parameters, except light transmission, are available. Also, international literature shows an extraordinary number of papers related to distribution, impact on native species, growth both in field or in laboratory under controlled conditions or on the production of alginates and fucoxanthin (Kane and Chamberlain, 1979, Arasaki and Arasaki, 1983, Rull Lluch et al., 1994; Bité, 2001, Britton-Simmons, 2004, Casas et al., 2004, Sánchez et al., 2005, Sánchez and Fernández, 2005, Davison, 2009, Baer and Stengel, 2010, Peng et al., 2011) but studies on the relationships with the local environmental parameters that might explain their spreading success are less common (Gorham and Lewey, 1984, Lewey and Gorham, 1984, Rico and Fernández, 1997) or relate to other similar species (Hwang et al., 2004).
The aim of this paper was to determine the monthly growth, the relative growth rate and the tissue concentrations of Sargassum muticum and Undaria pinnatifida in two different areas of the lagoon and correlate them with the most important environmental parameters of water column, pore-water, surface sediments and settled particulate matter (SPM). Finally, an estimate was made of the biomass of these brown algae comparing it with that of other invasive species present in the lagoon to identify the risk of anoxic events or other environmental impacts.
Section snippets
Study areas
Monthly sampling was carried out between March 2008 and February 2009 in two areas of the Venice Lagoon colonized by both Sargassum muticum and Undaria pinnatifida (Fig. 1). One station situated North-West of Venice was selected near the Gas island because of the presence of a methane plant in the historical centre (Gas st.: 45° 26′ 131″ N; 12° 17′ 564″ E). The station was close to the deep canal Vittorio Emanuele II that connects the industrial area of Porto Marghera to Venice. The bottom
Environmental parameters
The mean, standard deviation, maximum and minimum values of the considered environmental parameters (Table 1) recorded from March 2008 to April 2009 highlight the main differences between the two stations. Enel st. displayed a mean depth of 134 ± 21 cm, whereas Gas st. was ca. twice as deep (230 ± 22 cm). Depth influenced the light available on the bottom which was 637 ± 333 μE m−2 s−1 for Enel st. and 267 ± 180 μE m−2 s−1 for Gas st., i.e. 27% and 13% of the total (incident + reflected) light
Discussion
The Venice Lagoon is the basin of the Mediterranean Sea that presents the largest range of ecological conditions: from hyper-dystrophic to oligotrophic, from strongly influenced by the sea to confined or even close areas with very high temperature, salinity and water transparency changes and a massive presence of artificial substrata where NIS can found the better conditions for their growth. None of the NIS introduced in Venice Lagoon are spread everywhere but each of them occupies one or more
Conclusions
Sargassum and Undaria are two invasive alien species that in recent years have spread in the Venice Lagoon due to their big size and the massive colonization of banks and eutrophic areas around the historical centre of Venice and the city of Chioggia. The present study of their growth in two different areas supply additional information for the affinity of these species with environmental parameters, not only in the water column (temperature, light availability, nitrogen concentrations), but
References (48)
- et al.
Variability in growth, development and reproduction of the non-native seaweed Sargassum muticum (Phaeophyceae) on the Irish west coast
Estuarine, Coastal and Shelf Science
(2010) - et al.
Biological pollution in the Mediterranean Sea: invasion versus introduced macrophytes
Marine Pollution Bulletin
(2002) - et al.
Heavy metal contamination in seaweeds of the lagoon of Venice
Chemosphere
(2002) - et al.
Growth rate of Ulva rigida in different Mediterranean eutrophicated sites
Bioresource Technology
(2002) - et al.
Aspects of the ecology of Sargassum muticum (Yendo) Fensholt, in the Solent region of the British Isles. I. The growth cycle and epiphytes
- et al.
Organic micropollutants (PAHs, PCBs, pesticides) in seaweeds of the lagoon of Venice
Oceanologica Acta
(2003) - et al.
Decline of Ulva growth in the lagoon of Venice
Bioresource Technology
(1996) - et al.
Macrophyte production in a shallow coastal lagoon. Part I. Coupling with physico-chemical parameters and nutrient concentrations in waters
Marine Environmental Research
(1997) - et al.
Macrophyte production in a shallow coastal lagoon. Part II. Coupling with sediment, SPM and tissue nutrient concentrations
Marine Environmental Research
(1999) - et al.
Role of macroalgal biomass and clam fishing on spatial and temporal changes in N and P sedimentary pools in the central part of the Venice lagoon
Oceanologica Acta
(2003)