J Appl Phycol DOI 10.1007/s10811-015-0580-y
Environmental factors on egg liberation and germling production of Sargassum muticum Philip Kerrison 1 & Hau Nhu Le 2
Received: 11 November 2014 / Revised and accepted: 26 March 2015 # Springer Science+Business Media Dordrecht 2015
Abstract Sargassum muticum is a successful invasive Phaeophyte macroalga, which has colonized from Norway to the Mediterranean in Europe and from Alaska to the Bay of Mexico on the American Atlantic coast. It is also being evaluated as a commercial crop within its native range, SE Asia. Understanding its reproductive tolerance will improve our understanding of its invasive potential and allow optimal germling production for commercial cultivation. Egg liberation, fertilization and germling production were monitored in fertile branchlets collected from Great Cumbrae, Scotland, UK. These were incubated under a range of conditions as follows: photon flux densities (20–150 μmol photons m−2 s−1), salinity (0–70 psu), temperature (10–30 °C) and desiccation in either the sun (5–60 min) or the shade (15–120 min). The optimum conditions to maximize germling production were found to be a 15–30 min desiccation period in the shade, followed by immersion into normal salinity seawater at 20 °C and 50–100 μmol photons m−2 s−1. This information could be useful for the development of a cultivation industry within its native range. An interactive effect was seen between temperature and light intensity with germling production favoured in high light and low temperature (10–15 °C, 100–150 μmol photons m−2 s−1) and vice versa (25–30 °C, 20–50 μmol photons m−2 s−1). Whilst its salinity and desiccation tolerance agree with previous investigations 40 years ago, the lower
* Philip Kerrison
[email protected] 1
Scottish Association for Marine Science (SAMS), Scottish Marine Institute, Dunbeg PA37 1QA, Scotland, UK
2
Nhatrang Institute of Technology Research and Application (NITRA), Vietnam Academy of Science and Technology (VAST), 02 Hungvuong Street, Nhatrang City, Vietnam
temperature optimum of 20 °C (previously 25 °C) may indicate selection for lower temperature reproduction within the UK population. This may accelerate its invasion northward into Scotland. Keywords Sargassum muticum . Germling . Invasive . Temperature . Salinity . Irradiance . Desiccation
Introduction Sargassum is a brown algae genus containing 400+ species, with high diversity in Eastern Asia (Yoshida 1983). It forms extensive beds in the littoral regions which act as nutrient absorption beds, coastal protection and nursery and feeding areas for commercially important fish and invertebrates (Coston-Clements et al. 1991; Tsukidate 1992; Hwang et al. 2006). Sargassum muticum is native to Northeast Asia including Korea, where water temperature varies between 10 and 25 °C, and Japan (Yendo 1907), where it is confined to the warm waters of the Kuroshio Current (20–28 °C). Its native range is thought to be limited through outcompetition with the many other native Sargassum species (Critchley et al. 1983). S. muticum was first discovered on the south coast of England in the 1970s and has since spread rapidly across Europe, reaching Loch Ryan in Scotland in 2004 (Critchley et al. 1983; Davison 1996; Reynolds 2004). It is thought to have been transported to Europe through the importation of the Japanese oyster Crassostrea gigas (Farnham et al. 1973), with a recent study suggesting that the stock originated from Korea (Bae et al. 2013). It now ranges from Norway to Portugal and the Mediterranean (Engelen et al. 2008; Cheang et al. 2010). The monoecious species is characterized by high fecundity, with a long reproductive season, releasing a high number of
J Appl Phycol
relatively large propagules (Hales and Fletcher 1989). Male and female reproductive structures develop in separate conceptacles on the same receptacle. During reproduction, an egg is produced from each oogonium, which is exuded through the ostiole but remains bound to the adult by a mucilage sheath for several days (Fletcher 1980; Hales and Fletcher 1990; Kaur and Kumari 2012). This incubation period allows fertilization and initial germling development to occur whilst being attached to the adult. The sheath then degrades, detaching the non-motile germling which sinks rapidly, adhering to whatever substrate it encounters (Norton 1977, 1980; Fletcher 1980; Norton and Fetter 1981). This process only allows short-range dispersal. In the secondary dispersal method, detached branchlets or whole plants may become reproductive and release propagules whilst drifting, facilitating long-range dispersal (Norton 1977; Fletcher 1980). In a tertiary method, adults attached to small stones may move by peripatetic stone walking when the buoyancy and/or drag of the thallus exceeds the weight of the anchoring stone (Critchley 1981; Strong et al. 2006). Its varied dispersal methods are thought to have accelerated its spread throughout Europe and the American Atlantic coast. In SE Asia, many of the Sargassaceae are harvested for food, feed, fertilizer, chemical products and traditional medicine (Sohn 1993; Hong et al. 2007). Because of this, research has been conducted into the development of cultivation technology for many commercially harvested species including Hizikia fusiforme (Pang et al. 2005), Sargassum fulvellum (Hwang et al. 2006), Sargassum horneri (Pang et al. 2009), Sargassum naozhouense (Xie et al. 2013), Sargassum thunbergii (Zhao et al. 2008) and Sargassum vachellianum (Chai et al. 2014). These all share a similar life history, allowing the same propagation techniques to be utilized (Xie et al. 2013). So far, there has been little investigation into the possibility of commercial S. muticum cultivation in SE Asia (Cao et al. 2008; Liu et al. 2013). The impact of S. muticum colonization varies depending on the habitat characteristics and the native species assemblage (Salvaterra et al. 2013). It can cause dramatic changes, including the replacement of native species, alteration in the community flora and fauna, increasing sedimentation, reduced primary productivity and increased food web connectance (Salvaterra et al. 2013). An understanding of the environmental factors affecting egg/zygote release and early development of S. muticum will improve our understanding of this successful invasive, 40 years after its initial arrival in Europe. This may contribute towards controlling or predicting its further spread. Additionally, this information may contribute towards the development of its artificial seed production for aquaculture within its native range, as it has for other members of the genus (Pang et al. 2009).
Materials and methods Whole fertile specimens of Sargassum muticum were collected in August 2014 at ca 0.5–1.0 below chart datum from Great Cumbrae, Scotland (55° 45.211 N, 004° 54.070 W). These were transported to the Scottish Association for Marine Science (SAMS), Oban, in natural seawater within 3 h and then placed in 70 L outdoor holding tanks of aerated sandfiltered seawater. The thalli were gently cleaned of obvious epiphytic macroalgae and animals using a camel-bristled brush and rinsed several times in sand-filtered seawater. Two days following collection, distal branchlets, 6–8 cm in length with 10–12 receptacles, were selected for the experiments. These were cleaned again using a brush and washed several times with Tyndallized seawater (Kawachi and Noël 2005). Depending on the experiment, three or five branchlets from the same individual were placed into either Petri dishes containing 20 mL or plastic pots containing 400 mL of culture medium in triplicate. The medium was composed of Tyndallized seawater (32 psu) enriched with F/2 media without silicate and 0.125 mg L−1 germanium dioxide to prevent diatom growth (Markham and Hagmeier 1982). After the beginning of each experiment, egg liberation was examined daily using a dissecting microscope. The data reported show results after 4 days when 100 % egg liberation was first observed. Measurements were made of the percentage of receptacles showing egg release (n>30), the number of liberated eggs was counted using a Sedgewick-Rafter counting slide (n=3), and the percentage of eggs which were fertilized was also determined. Temperature and light The combined effect of temperature and light was examined in triplicate under five temperature (10, 15, 20, 25 and 30 °C, ±0.5 °C) and four irradiance regimes (20, 50, 100 and 150 μmol photons m−2 s−1) with a 12:12 h, light/dark cycle in 400 mL containers. Temperature was controlled using temperature controllers (WH7016; Willhi, China) linked to a thermocouple and 100–200 W water heaters. Lighting was provided by overhead fluorescent lights using plastic sheeting or mesh covering to reduce light intensity. Salinity Sodium chloride was added to Tyndallized seawater (psu) to reach a salinity of 70 psu, determined using a refractometer (Atago, Japan). Ultra high-purity water was added to create a range of salinities. Egg liberation was examined in 20 mL volumes at 10 psu increments between 0 and 80 psu. These were incubated for 4 days at 22 °C and 50 μmol photons m−2 s−1 with a 12:12 h light/dark cycle.
J Appl Phycol
Desiccation Receptacles were blotted dry with tissue and were then exposed to either low light (
