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Growth, artificial seedling raising and cultivation of Sargassum confusum (Fucales, Phaeophyceae) inhabiting the coast of Shandong Peninsula, China

  • Jinhua Pan
  • Zhuangzhi Zhang
  • Shenhui Yu
  • Houwei Han
  • Xin Jiang
  • Liming Jiang
  • Guangjin Liang
  • Juan Sun
  • Xiaojie LiEmail author
  • Guanpin Yang
Article

Abstract

The seasonal growth, seedling raising and artificial cultivation of Sargassum confusum were studied along the coast of Dong Chudao at the mouth of Sanggou Bay (37°02′12″N, 122°33′51″E). We also compared the growth of juveniles at different temperatures (15, 18, 21, and 24 °C) and irradiances (60, 95, and 130 μmol photons m−2 s−1) when seedlings were raised in a greenhouse. Sargassum confusum in Sanggou Bay began to develop receptacles in early April when the seawater temperature reached 10.8 °C. The receptacles matured in July and released the eggs when the seawater temperature reached 21 °C. The S. confusum thallus grew to maximum mean length (126.6 ± 19.8 cm) and reached the highest mean biomass yield (192.2 ± 40 g dwt thallus−1) in July and then rapidly decayed. Both temperature and irradiance significantly affected the growth of S. confusum seedlings (p < 0.05). The seedlings reached 1005 ± 47.6 μm at 21 °C and under 95 μmol photons m−2 s−1 in 2 weeks. The seedlings grew to approximately 0.5 cm in length in the seedling raising pools in approximately 5 weeks and reached 6 cm in the open sea nursery after an additional 4 months. The seedlings were then separated and inserted between the strands of vinylon ropes and cultivated in the open sea until early July when the seawater temperature reached approximately 21 °C and the maximum thalli length reached 116.4 cm on average. The dry weight of S. confusum harvested from a 4-m cultivation rope was 1.48 kg on average, and the dry weight yield was approximately 8.9 t ha−1.

Keywords

Seasonal growth Artificial seedling raising Cultivation Sargassum confusum Phaeophyta 

Introduction

Sargassum C. Agardh, one of the most species-rich and ecologically important brown algal genera, is conspicuously distributed along the subtropical and tropical coasts, especially those of China, Korea Peninsula, and Japan (Yoshida 1983; Tseng 1984; Phillips 1995; Lee and Kang 2002). The species in this genus play critical roles in ocean ecosystems by forming natural seaweed beds and even the Sargasso Sea, thus providing essential habitats for epiphytes, fish and crustaceans (Sehein et al. 2014; N’Yeurt and Iese 2015). Compared with the well-developed seeding and cultivation techniques of Saccharina, the seedling raising and cultivation techniques of Sargassum are still limited. During early studies, holdfast-derived regenerated seedlings and juvenile thallus from wild populations were used to cultivate Sargassum (Hwang et al. 1998; Zou et al. 2005). The perennial holdfasts from the previous year’s thallus could be reused (Hwang et al. 1998). Then, Sargassum seedlings were obtained from reproductive thalli through sexual reproduction and the yield increased (Pang et al. 2001). From then on, the seedling raising and cultivation techniques used for Sargassum began to develop gradually. The growth and maturation of Sargassum fulvellum from the southwestern coast of Korea was surveyed and its embryo paintbrush seedling raising and cultivation technique was successfully developed (Hwang et al. 2006). The optimal growth temperature and irradiance conditions for Sargassum were evaluated and the early development of Sargassum thunbergii germlings from the coast of Qingdao, China, was observed under laboratory conditions (Zhao et al. 2008). The Sargassum horneri cultivation technique was developed and the life cycle was shortened to 4.5 months (Pang et al. 2009). Zhang et al. (2012) studied the zygote-derived seedling production of S. thunbergii and developed practical techniques to manage its appropriate seeding density and jet-washing pressure. The artificial seed production and cultivation of Sargassum naozhouense were successfully trialed, and the yield reached 1750 kg wet wt km−1 (Xie et al. 2013). The impacts of substrate variations on the vegetative growth of Sargassum echinocarpum spores were tested, which provided reference information for the selection of substrate material when raising Sargassum seedlings (Hamza et al. 2016). As an introduced alga floated to northern Taiwan, the germling survival ability of S. horneri was tested under different temperatures (Lin et al. 2017).

The population structure and dynamics of Sargassum confusum have been well studied in Korea and Japan (Koh and Shin 1990; Tsuda and Akaike 2001). Sargassum confusum was also used to construct an algal bed (Chai et al. 2014; Kang et al. 2016). In China, S. confusum is usually used as feed for sea cucumber. However, ecological studies on this species are scarce and seedling raising has rarely been attempted in China. In recent years, the rapid expansion of sea cucumber aquaculture has led to the depletion of natural S. confusum populations along the northern coast of China. In addition, the recovery of the natural beds of this species using the currently available techniques seems to be ineffective and unsustainable (Leung et al. 2014). Such circumstances make it necessary to develop an efficient seedling raising technique, thus realizing the artificial cultivation of this algae.

In this study, we traced the growth and sexual reproduction season of S. confusum in nature and determined the temperature and irradiance requirements for the early growth of S. confusum under laboratory conditions. In addition, an artificial seedling raising method was developed, and open sea cultivation of raised seedlings was trialed. This research will provide practical guidelines for the mass artificial seedling raising and commercial cultivation of S. confusum.

Materials and methods

Study site

The study site was on the southern coast of Dong Chudao at the mouth of Sanggou Bay (37°02′12″ N, 122°33′51″ E), which is located on the east coast of Shandong Peninsula, China. Sargassum confusum grows dispersedly on the hard substrate of rocks and boulders in the lower intertidal or subtidal zone as a partial mixture with Sargassum thunbergii, forming algal meadows along the coast.

Field surveys

Field surveys were carried out from March 2010 to February 2011. The water temperature and salinity were recorded every day. Ecological surveys usually occurred in the middle of each month at low tide. In total, 30 S. confusum thallus were randomly sampled by a scuba diver using a knife to pry the holdfasts of the thallus from rocks or stones. The sampled thalli were packed into a foam box with ice bags and transported to the laboratory in 3 h. All sampled thalli were measured for length and dry weight. The dry weight was obtained after drying at 65 °C to a constant weight. Apical fragments from 5 random specimens were preserved in silica gel for DNA extraction. DNA extraction, amplification, and sequencing analysis were performed using the methods described by Huang et al. (2017).

Effects of temperature and irradiance on seedling growth

During the reproductive season, the receptacles (together with lateral branches) bearing released embryos (embryos still attached to the surface of the receptacles and had not been liberated) were collected and immediately transported to the laboratory. Then the receptacles were rinsed with sterilized and filtered seawater and placed into a 10-L water tank with sterile seawater. After being liberated from the receptacles, the embryo suspension was concentrated to approximately 300 embryos mL−1. The suspension was allocated into Petri dishes (ø10 cm), 2 mL each. The Petri dishes containing embryos were cultured in four incubators (MGC-100, Bluepard China) with the temperature and irradiance conditions set following a full-factorial ANOVA experimental design. Seedlings were exposed to three irradiances (60, 95, and 130 μmol photons m−2 s−1) at four temperatures (15, 18, 21, and 24 °C). Irradiance was measured using an irradiance meter (3415F, Spectrum, USA). Three Petri dishes (3 replicates) were allocated to each treatment. All treatments were set at a 12:12 h (L:D) cycle. PESI was used as the cultivation medium and replaced every 3 days. The experiments lasted 2 weeks, and the seedlings were photographed using an inverted microscope (Olympus IX51), and their lengths, excluding the rhizoid, were measured using Image-Pro plus. Thirty seedlings from each Petri dish, 90 in total, were measured in each treatment.

Artificial seedling raising and cultivation trial

On 16 July 2014, the reproductive thalli were collected and immediately transported to the algal seedling cultivation base. Upon arrival, the reproductive thalli were kept in water tanks containing fresh filtered seawater which was continuously aerated and stirred. Usually, after 5–12 h, a large number of liberated embryos settled to the bottom of the tank. The reproductive thalli were then transferred to another water tank to liberate more embryos. The liberated embryos that sank to the bottom of the water tank were collected by a 200-mesh sieve (pore size, 80 μm). First, the embryos were filtered by a 30-mesh sieve (pore size, 600 μm) to remove large impurities and debris. Second, the embryos were washed repeatedly with fresh filtered seawater until the rinsed water became clear to remove most diatoms and spores of wild seaweeds. Finally, the dense embryo suspension was ready for attaching to the collector. Vinylon rope collectors were used for embryo attachment. Each collector was framed with PVC (30 cm width × 56 cm length, holding a total length of 37 m vinylon rope with a diameter of 3 mm) and fixed to the bottom of a concrete pool. Before fixation, the collectors were soaked in fresh filtered seawater for 3 days with the fresh filtered seawater being fully replaced every day. The concrete pool used for the seedling cultivation was 2.3 m in width, 8.5 m in length, and 40 cm in depth. Fresh filtered seawater was continuously supplied, and the seawater flow was adjusted dynamically according to the actual requirements.

After 5 weeks of pool cultivation, the seedlings were transferred to the open sea nursery area. After the high-temperature season, the seedlings grew to a certain length in December, and the seedlings were separated and fixed on a vinylon cultivation rope, 4 m in length and 2 cm in diameter. Then, the cultivation was carried out using methods similar to those used to cultivate kelp at sea (Li et al. 2007). The length of the thalli and seawater temperature were continuously recorded during cultivation. The yield (t ha−1, 6000 ropes per hectare) was calculated in the harvest season.

Data analysis

Two-way ANOVA was performed to assess the main effects of temperature and light intensity on seedling growth. Leven’s test of homogeneity of variances was performed to check the assumption of parametric statistics in ANOVA. The parametric assumptions of the statistical models were evaluated, and the data were transformed if necessary to fit these assumptions. The significance level was set at 0.05. All analyses were performed with SPSS 17.0 for Windows.

Results

Seasonal growth of wild S. confusum

Sequence similarity searches were performed against the National Center for Biotechnology Information (NCBI) database using the BLAST program. The ITS-2 and cox3 sequences of 5 random specimens were consistent with Sargassum confusum C. Agardh (GenBank: KY411080 and KY411106).

Beginning in April, the length and dry weight of S. confusum increased rapidly, reaching an average maximum of 126.6 ± 19.8 cm and 192.2 ± 40 g thallus−1 (dry wt), respectively, in July, and then the alga started to decay (Fig. 1).
Fig. 1

Seasonal growth of thallus length and dry weight of S. confusum inhabiting the coast of Dong Chudao in the Yellow Sea (mean ± SD, n = 30)

The monthly average temperature ranged from 1.2 °C in January to 23.1 °C in August, and the average salinity ranged from 31.5 to 33.5 psu in situ (Fig. 2). The receptacles were first discovered in early April when the seawater temperature was 10.8 °C. This condition indicated the beginning of the reproductive season (shadow area in Fig. 2). The disappearance of the receptacles in early August marked the end of the reproductive season when the seawater temperature was 23.5 °C. The peak reproductive period was indicated by the release of the largest amount of eggs from the receptacles from late June to early July when the seawater temperature varied between 18.5 and 20 °C. This period was also the optimum opportunity to start artificial seedling raising.
Fig. 2

Water temperature and salinity variations in situ (mean ± SD, n = 28). Shaded area indicates the sexual reproduction period in nature

The annual branches have numerous small round or slightly pear-shaped air vesicles (Fig. 3a, b), which help the thalli stand in the seawater. The adult branches with receptacles bearing zygotes (in July, Fig. 3c) liberated the embryos (Fig. 3d). After being liberated, the embryos sank and immediately reattached to any surface encountered by the rhizoids. After 3 days of growth, the embryo’s rhizoids (Fig. 3e) reached approximately 300 μm. After 5 weeks of growth, juvenile seedlings grew to approximately 5 mm (in August, Fig. 3f) and reached approximately 6 cm after an additional 4 months in December (Fig. 3g). Then, the thalli grew until the following July and started sexual reproduction again. Figure 3h shows the entire thalli in the nonbreeding season.
Fig. 3

Life cycle and morphological characteristics of S. confusum. a Annual branches. b Air vesicles (a) and receptacle (b). c Receptacle bears zygotes (c). d Liberated embryos. e Juvenile seedling with rhizoids (d). f Juvenile seedlings after 5 weeks of growth. g Seedlings after approximately 5 months of growth. h The entire thallus in the nonbreeding season

Effects of temperature and irradiance on seedling growth

Both the tested temperature and irradiance significantly affected seedling growth. After 2 weeks of cultivation at 21 °C and 95 μmol photons m−2 s−1, the mean seedling length reached a maximum of 1005 ± 47 μm on average (Fig. 4), which was significantly longer than that in the other groups (two-way ANOVA, p < 0.05).
Fig. 4

Seedling length after 2 weeks of cultivation at different temperatures and irradiances. a 60 μmol photons m−2 s−1. b 95 μmol photons m−2 s−1. c 130 μmol photons m−2 s−1. Different lowercase letters above bars indicate significant differences (p < 0.05, ANOVA) (mean ± SD, n = 90)

Artificial seedling raising

The collectors were fixed to the bottom of the cultivation pool filled with fresh filtered seawater. The embryo suspension was diluted to approximately 200 embryos mL−1 and evenly sprayed onto the surface of the seawater (Fig. 5d, e). The embryos then settled onto the collectors. Approximately 30 L of embryo suspension was evenly sprayed in each pool, which ensured an initial density of approximately 30 embryos cm−2. For 98 collectors in one pond, at least 5 kg of parental thallus were needed. After 24 h, the seawater flow (approximate flow velocity, 8–10 cm s−1) in the pool was initiated.
Fig. 5

Artificial seedling raising. a Parental thallus in the water tanks. b Embryo collecting and concentrating using a 200-mesh sieve. c Embryo rinse. d Dense embryo suspension. e Embryo spraying. f Juvenile seedlings on the collector after 1 week of growth

During the period of seedling cultivation in the pool, irradiance was regulated through a regulating system composed of a bamboo curtain and a layer of plastic mesh on top of the fiberglass ceiling of the greenhouse. At the beginning of seedling raising, the average irradiance was set at 90–120 μmol photons m−2 s−1. With the growth of the seedlings, irradiance was gradually intensified. From the third week, the average irradiance was increased by approximately 20 μmol photons m−2 s−1 every 2–3 days. The first spray washing began 3 days after embryo attachment. The seawater spraying pressure was relatively lower at the beginning and increased gradually with the increase in the adhesion force of the seedlings (Fig. 6a). Practical experiences have revealed that the spraying pressure of the seawater wash should be less than 0.03 MPa for the first wash, which should be increased gradually to 0.15 MPa with the development of seedlings.
Fig. 6

Seedling management and cultivation. a Spray washing. b Juvenile seedlings after 5 weeks of growth. c Seedlings fostering on the sea on 19 December 2014. d Adult thallus cultivated on the sea on 6 May 2015

Artificial cultivation

On 21 August 2014, 5 weeks after seeding, the seedlings grew to approximately 0.5 cm (Fig. 6b), and the density was approximately 12 seedlings cm−2. The seedling survival rate was approximately 40%. Then, the seedlings were transferred to the open sea nursery cultivation area. The average irradiance increased to approximately 300 μmol photons m−2 s−1. The seedlings needed to be exposed to an average irradiance lower than 350 μmol photons m−2 s−1 during the first 2 days. Accordingly, the seedling collectors were hung horizontally at a depth of 40–60 cm (depending on the transparency of the seawater) in the open sea nursery. In the early period after being transferred to the sea area, spray washing was carried out every 2 days to prevent the attachment of epiphytic algae and other unpredictable, hostile organisms and muddy sand. On 28 December 2014, the seedlings had grown to approximately 6 cm in length (Fig. 6c) and were separated and fixed (inserted) to the vinylon cultivation rope, with 20 seedlings on each rope. The cultivation rope was 4 m in length and 2 cm in diameter. The seedlings were evenly fixed and horizontally cultivated in the sea at a depth of 50 cm until early July 2015 when the seawater temperature reached approximately 21 °C, and the thallus grew to 116.4 cm on average (Fig. 7). The mean dry weight of S. confusum for one cultivation rope was 1.48 kg. An average of 18 thalli were left on the cultivation rope in July, so the mean individual dry weight was approximately 82.4 g. The dry weight yield was approximately 8.9 t ha−1.
Fig. 7

Length of Sargassum confusum thallus cultured in the open sea (mean ± SD, n = 30)

Discussion

Artificial seedling raising

Stable and sufficient supply of seedlings is the premise for commercial-scale cultivation of Sargassum (Xie et al. 2013). Supply of holdfast-derived regenerated seedlings and young thalli from wild populations was once used for farming (Hwang et al. 1998; Zou et al. 2005). However, the two methods were unsustainable and cannot meet the demands of commercial-scale farming because they resulted in severe destruction to the natural Sargassum resources. The sexual reproduction breeding methods that used to produce Sargassum seedlings had been widely documented (see review by Kim et al. 2017), and this has been proved to be a sustainable way for commercial farming of Sargassum. The attachment of diatoms on the seedlings in the collectors is a considerable problem when the seedlings are raised in a greenhouse. The diatoms attached to the seedlings compete with the seedlings for nutrients, irradiance, and other resources, which may cause a high rate of detachment of the seedlings from the collectors. Preventing the attachment and excessive multiplication of diatoms is critical for ensuring the success of raising S. confusum seedlings. Spray washing is usually adopted as an effective method of removing diatoms from seedlings to suppress excessive multiplication. Spray washing should also promote the development of seedling rhizoids, aiding seedlings to fix more firmly to the embryo collectors (Pang et al. 2006).

Seasonal growth: wild and artificially cultivated thallus

The growth of S. confusum inhabiting the east coast of Shandong Peninsula begins in spring and ends when sexual reproduction ends in early August. Tsuda and Akaike (2001) divided the annual life cycle of S. confusum inhabiting the coast of Hokkaido, Japan Sea, into four periods: slow growing, rapid growing, mature, and withering. The same growth rules were also discovered in the S. confusum population surveyed in this study. As is the case for many marine algae species, the sexual reproduction of S. confusum usually occurs at the end of growth. Maturation is not simultaneous; the first mature thallus completes its growth while the non-reproductive thallus continues to grow (Norton 1977; Arenas and Fernández 1998; Pan et al. 2011). In this study, the S. confusum maturation season began in early April, and thalli growth continued until July. The peak sexual reproduction of S. confusum at the survey site continued from late June to early July when the seawater temperature varied from 18.5 to 20 °C. Later, the thallus withered. As shown in this study, both the wild and artificially cultivated thallus reached the maximum average length in July. The maximum length of wild thallus was 126.6 cm on average, while that of cultivated thallus was 116.4 cm. Meanwhile, the peak dry weight of individual wild thallus was 192.2 g, which was much higher than that of the cultivated thallus (82.4 g). Water temperature, irradiance, nutrient concentration and composition, exposure time in the intertidal zone, and wave action are considered to be responsible for the variations in the growth and yield of Sargassum spp. (Engelen et al. 2005; Hwang et al. 2007; Sun et al. 2009; Baer and Stengel 2010). The artificial cultivation sea area in this study was only hundreds of meters offshore from the wild population sampling site. Therefore, the nutrient and temperature conditions were nearly the same. However, the wave action and exposure time were different because the habitat of the wild population was exposed to daily tides, while the artificially cultivated thalli were not exposed to tidal variations. Baer and Stengel (2010) discovered that the biomass of Sargassum muticum produced in a sheltered tide pool was 3.5 times lower than that of the thallus on an open shore. The results of this study are in line with this conclusion.

Artificial cultivation in open sea

Algal cultivation usually results in less negative environmental impacts than algal harvest from wild populations (Kapraun 1999). The mass production of embryos at a commercial scale and the successful seedling raising on the collector developed in this study make the large-scale cultivation of S. confusum practical.

At the early stage after the seedlings were transferred to the open sea, several factors were considered to be responsible for the detachment of Sargassum seedlings from the collector. Photodamage (e.g., strong UV irradiation) may have occurred when the seedling collectors were hung horizontally beneath the sea surface. According to a study on Hizikia (Sargassum) seedling raising, attachment was not damaged when the seedlings were exposed to direct solar irradiance for no more than 2 h. The longer the seedlings were exposed to high irradiance, the more severe the photoinhibition in the seedlings (Pang et al. 2007). The depth at which the collectors were hung is a decisive factor that determines the actual level of photosynthetically active radiation and UV radiation on sunny days and thus affects the cultivation yield (Hwang et al. 2007). According to our experience, the actual illumination received by the seedlings should be no more than 300 μmol photons m−2 s−1 in the first 2 days after being transferred to the open sea nursery area. The specific depth depended on the transparency of the seawater in the open sea where the seedlings were nursed. Usually, a depth of 50 cm was appropriate in Sanggou Bay in the Yellow Sea.

Another problem after the seedlings were transferred to the open sea nursery area was the mud and silt that sank to the collectors and deposited on the surface of the seedlings. This condition reduced the irradiance that reached the seedlings and thus caused a high rate of detachment. Spray washing is critical for keeping the seedlings clean, especially at the early stage when the seedlings were newly transferred to the open sea nursery. Spray washing could also promote the development of seedling rhizoids, aiding the seedlings to fix more firmly to the collectors, thus increasing the resistance of young seedlings to adverse open sea environmental stresses.

Conclusions

Sargassum confusum inhabiting the coast of Shandong Peninsula, Yellow Sea, develops its receptacles at the beginning of April. The receptacles mature in July, and the biomass of S. confusum sporophytes simultaneously peaks. The receptacles disappear in early August, which indicates the termination of continuous but not synchronized sexual reproduction of S. confusum. Both temperature and irradiance significantly affect the growth of S. confusum seedlings. The temperature and irradiance conditions should be controlled during the early growth of S. confusum. Artificially raising seedlings in a greenhouse and the open sea cultivation of S. confusum are feasible. Such practices should help protect this natural resource. During the cultivation trials, the maximum thalli length reached 116.4 cm on average, and the dry weight yield reached 8.9 t ha−1.

Notes

Acknowledgments

We wish to thank the two anonymous reviewers for their valuable comments on this manuscript. We also wish to show our appreciation to Z.M. Sun, from the Institute of Oceanology, Chinese Academy of Sciences, for his kind assistance in taking the photo of the entire S. confusum thalli.

Funding information

This work was supported by China Agriculture Research System (CARS-50), the National Technical Supporting Project Foundation (No.2012BAD55G01), and the Special Funds for Key Laboratories Construction of Shandong Province (No. SDKL2017009).

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Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Jinhua Pan
    • 1
  • Zhuangzhi Zhang
    • 1
  • Shenhui Yu
    • 1
  • Houwei Han
    • 1
  • Xin Jiang
    • 1
  • Liming Jiang
    • 1
  • Guangjin Liang
    • 1
  • Juan Sun
    • 1
  • Xiaojie Li
    • 1
    Email author
  • Guanpin Yang
    • 2
  1. 1.Key Laboratory of Algae Genetic Breeding and Cultivation Techniques of Shandong Province, National Algae and Sea Cucumber Engineering and Technique Research CenterShandong Oriental Ocean Sci-Tech Co., Ltd.YantaiChina
  2. 2.College of Marine Life SciencesOcean University of ChinaQingdaoChina

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