Bingxin Huang, Yue Chu, Rongjuan Wang, Yixiao Wang, Lanping Ding. Effects of main ecological factors on the growth of marine green alga Caulerpa sertularioides using the response surface methodology[J]. Acta Oceanologica Sinica, 2023, 42(11): 90-97. doi: 10.1007/s13131-023-2171-0
Citation: Bingxin Huang, Yue Chu, Rongjuan Wang, Yixiao Wang, Lanping Ding. Effects of main ecological factors on the growth of marine green alga Caulerpa sertularioides using the response surface methodology[J]. Acta Oceanologica Sinica, 2023, 42(11): 90-97. doi: 10.1007/s13131-023-2171-0

Effects of main ecological factors on the growth of marine green alga Caulerpa sertularioides using the response surface methodology

doi: 10.1007/s13131-023-2171-0
Funds:  The National Natural Science Foundation of China under contract Nos 31970216, 32270219 and 31670199.
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  • Corresponding author: E-mail: skydlp@tjnu.edu.cn
  • Received Date: 2022-10-25
  • Accepted Date: 2023-01-11
  • Available Online: 2023-09-18
  • Publish Date: 2023-11-01
  • Caulerpa sertularioides is an invasive potential blooming green alga in China but it remains poorly studied. We studied the effects of ecological factors on its growth. Optimum conditions of ecological factors, i.e., irradiance, temperature, and salinity, for the growth of its fragments were determined in the response surface methodology (RSM). The specific growth rates (SGR) of the fragments were determined in single-factor experiment. The results show that the SGR of C. sertularioides peaked under the conditions of irradiance 37.5 μmol/(m2·s), temperature 25℃, and salinity 30. Meanwhile, using the Box-Behnken design, the conditions were further optimized and verified to be: irradiance 39.03 μmol/(m2·s), temperature 25.29℃, and salinity 30.06, under which the SGR reached 4.66%. The results provide new theoretical data and solutions for the cultivation, invasion prediction, and monitoring of Caulerpa species in China and the world. The RSM method may have great potential applications in the environmental adaptation characteristics of new macroalgal cultivars, intensive orientation cultured germplasm, and environmental hazard analysis of cultivated species in the field.
  • Acoustic seafloor characterization, which enables to map the wider areas faster, has been a very useful tool for the imaging the seafloor features and provides important data for marine geology studies, hydrography, marine engineering, and environmental sciences etc. The advantages of high-resolution seafloor imaging with large swath widths compared to conventional seafloor sampling methods (such as grab, core sampling, Bull et al., 1998) are saving time from the survey and minimizing the costs. However, especially for the sediment distribution mapping studies, the different reflections from the seafloor should be identified with the conventional methods or previous studies, if enabled.

    The side scan sonar (SSS) system, which provides high-resolution imaging of the seafloor with nearly photographic quality and great swath range, is one of the effective acoustic methods. It is beneficial for detecting geological structures (such as outcrops, faults) that cause acoustic differentiate on the seafloor and also very useful in the sediment (sand, clay, gravel, mud, etc.) classification of the seafloor according to backscattering strength (Richardson et al., 2001; Briggs et al., 2001; Goff et al., 2004; Ferrini and Flood, 2006; Buscombe, 2017). Finer sediments that have high porosity, low density and sound velocity can be determined by the low backscatter intensity. In contrast, coarser sediments that have lower porosity cause increases in both density and velocity and therefore are more likely to result in higher backscatter intensity. There are important caveats to consider with respect to grain size effects on backscatter intensity including, the possible presence of near-surface gas in muddy sediments that can result in increased backscatter intensity (Borgeld et al., 1999, Fonseca et al., 2002). Similarly, fine-grained surface sediments underlain by subsurface layers of coarser sediment can exhibit high acoustic backscatter intensity because of subsurface changes in impedance contrast. The presence of subsurface inhomogeneity induced by bioturbation can also result in high backscatter intensity in fine-grained sediments (Urgeles et al., 2002). Seabed surface roughness is an important variable to consider with respect to high-frequency acoustic backscatter intensity and has been investigated by several researchers (Stewart et al., 1994; Briggs et al., 2001; Richardson et al., 2001). The effects of roughness on backscatter intensity vary depending on the type, magnitude, and orientation of roughness as well as the frequency of the acoustic signal. In addition, using SSS is very useful in detecting wrecks, ruins, and deformations on the seafloor (Barnhardt et al., 1998; Grindlay, 2009; Collier and Brown, 2005; Dumanoğlu, 2014).

    Sediment transport, deposition and erosion mechanisms are particularly effective in wave shoaling, breaking and surf zones. The usage of the coastal and near shore areas caused changes on these hydrodynamic affects. Throughout history, civilizations have generally preferred to settle close to coasts because the sea is an important source of food, energy useful for transportation, and other marine economic fields. It has been an important and intensively used area in the world for a long time since it plays an important role in the social economy (Arthur, 1996; Auer, 1997; Chen, 1998; Cicin-Sain and Knecht, 1998; Gayr and Klee, 1999). On one hand, the deltas formed by the deposition of the terrigenous materials carried by the rivers in the coastal areas and the productivity of these soils were the biggest factors for the settlements in these regions. On the other hand, the mooring effects of large and/or small boats, ships, etc. that play a role in maritime trade, mostly cause deformations and abrasions on the seafloor. In addition to the deformation and abrasion on the seafloor and near the coastal areas sourced to the construction of the coastal engineering structures such as fishing port area, marinas, and breakwaters, can cause formation of morphological structures such as sand bars, barrier islands and/or disappearance or sudden appearance of beach areas. These are the main problems about the usages of the coastal areas because shallowing of the sea caused problems on ship traffic, changes of the beach areas are the directly related with the coastal management and tourism; the seafloor deformations or formation of the sandbars, barrier islands provided significant changes on the habitat. Therefore, understanding, revealing the occurrence, and offering scientific solutions to these problems are becoming more and more important.

    To protect the sustainability of the benefits from our seas and near coasts, which have very complex hydrodynamic conditions without disrupt the balance of nature, it is necessary to approach the problem scientifically by considering the environmental effects. Therefore, the construction planning of coastal civil structures and zones should be done coherently with nature and be eco-friendly, and so the minimum environmental impact should be taken into consideration.

    The main purpose of this study is to define the seafloor features in the nearshore marine areas that are currently in intensive use, determine the anthropogenic impacts and reveal the effects on the seafloor. Thus, this study will be an important reference for understanding the effects and risk factors of the usages that made or planned to be made in coastal and/or near coastal areas. For this purpose, coastal marine areas at western Istanbul (between Küçükçekmece-Büyükçekmece lagoons, Fig. 1) was chosen as a study area because of its high level of settlement which has been used extensively as social life and trade center from past to recent. Furthermore, pressure of terrestrial input, ship traffic, marine engineering structures, and port activities also lead to the selection of this study area.

    Figure  1.  Location (a), bathymetry (b), regional geology maps (c) of the study area (modified from Alp et al. (2018)). NAF: north Anatolian Fault, EAF: east Anatolian, TEF: Tharace Eskişehir Fault, BF: Büyükçekmece Fault, OAF: Offshore Avcılar Fault.

    The coastal area between the Küçükçekmece–Büyükçekmece lagoons of Istanbul has a length of about 20 km and has attracted the attention of humankind in tourism activities, industry, maritime trade, fishing, etc. for centuries. These lagoons are ancient estuaries and connected to the Sea of Marmara through narrow canals in the region (Salar et al., 2021). Their connection with the sea was cut by the sand bar, which were formed by currents and wave systems and lagoon conditions created in the early 20th century with man-made reinforcement barriers. An ancient port was reported (Öniz et al., 2014) between these lagoons which had been settled between these lagoons during BC 4th to AC 10th centuries. In addition, the ancient city of Bathonea was reported in the Küçükçekmece Lagoon (Aydıngül, 2013). Ambarlı harbor, west Marine Marina, Gürpınar fishing port, associated breakwater structures and pipelines at the recent contractions placed on the seafloor and the coast.

    The shelf of the study area is generally low sloped, it suddenly deepens from the shelf break with a high slope and is compatible with the general morphology of the Sea of Marmara (Gazioğlu et al., 2002). The widest shelf which covers approximately 15 km is among the Büyükçekmece Bay and offshore extensions of the river outputs from the coast can be seen in Fig. 1. Subhorizontal sea bottom morphology has irregular bathymetric features and narrow canyons around the lagoons of Büyükçekmece and Küçükçekmece. Due to the valley structure in Büyükçekmece Bay, the submarine morphology is unique to the northern Marmara Shelf (Ergintav et al., 2011; Nasıf et al., 2019). The valley’s formation had been controlled by an inactive fault and it is the major evidence that shows the ancient stream coming from Büyükçekmece Lagoon (Vardar et al., 2018). The region offshores the gulf of Büyükçekmece bay has a complex morphology if compared to the region offshore the lagoon of Küçükçekmece. Rock outcrops identified in seismic datasets (Alp et al., 2018) indicate tectonic compression and high erosion. The depth of the outcrops is at 85 m and are presented as wave-cut terraces (Alp et al., 2018). The outcrops on the edge of the Büyükçekmece valley are also associated with the decreasing on the sea level and are at the same levels as the old deltas around the Büyükçekmece valley (Vardar et al., 2018).

    The acoustic reflection dataset was acquired with the DeepVision DE3468D Dual CHIRP Digital 340/680 kHz SSS system in 2017. To provide high quality dataset by considering the features of seafloor morphology, the 340 kHz frequency and 128 000 baud-rate operation settings were utilized. Wavelength is about 4 mm, theoretically minimum along-track resolution is of about 1.5 cm (calculated assuming a horizontal beam width 0.9°) and swath-range is 150 m (total 300 m). The 6 m long zodiac boat was used, and the boat speed was fixed as an average of 2−2.5 knots. In the study area, SSS data were collected in accordance with the coastal morphology as permitted by ship traffic (Fig. 3).

    The following basic data processes were applied to the SSS data. Pre-processing, the conversion of the recording format to the program format. Main processing, this process covers radiometric (calibration), mosaic processes. Post-processing, it provides to increase the quality by eliminating noises.

    The seafloor sediment identification was made according to Barnhardt et al. (1998), the definitions of the main units’ reflection are given in Table 1.

    Table  1.  Acoustic returns and the outcrop features of the seafloor formations
    Map unit Acoustic reflection
    intensity
    Outcrops features
    Mud (M) weak smooth flat
    Sandy Mud (SM) weak smooth flat
    Muddy Sand (MS) medium smooth flat
    Sand(S) medium smooth flat
    Gravel (G) strong low relieve often covered with
    ripples or boulders
    Rock (R) strong high relief, fractures common
     | Show Table
    DownLoad: CSV

    Also, the intensity values obtained by the acoustic signals produced by the side-scan sonar reflecting from the seabed and returning to the receiver vary according to the sediment unit. These value ranges are in different colors and each range shows a different sediment unit (Fig. 2). These unit ranges were obtained from the SonarWiz program (Pratomo et al., 2018). These reflections and amplitude values were determined from the collected acoustic data. Afterwards, the boundaries where they overlapped and correlated with previous studies were mapped.

    Figure  2.  Acoustic returns of the seafloor formations.

    Depending on the reflection intensities (weak to strong), the color scale ranges from very dark brown to light brown. The intensity of reflection and the darkness of the color are inversely proportional, and the seafloor formation with the weakest reflection density and the darkest color is “Mud (M)”. Depending on the decrease in the reflection density and the gradual lightening of the color, the sediment sequence continues as “Sandy Mud (SM), muddy Sand (MS), Sand (S), and Gravel (G)”. The seafloor formation with the strongest reflection intensity and the lightest color (light brown) is “Rock (R)” (Table 1, Fig. 2).

    The sediment distribution maps of the study area, which were previously presented in Oktay (1998), Olgun (2001), Alpar et al. (2014), were used for the ground trawling of acoustic data. Those maps were acquired from the conventional sediment sampling methods, and the gaps between sampling locations were filled by the computer interpolations. According to the correlation of two data sets (acoustic and sediment sampling), the borders of the different sediment formations can be mapped more accurately.

    The bathymetry map of the study area given in Fig. 1b was obtained from high-resolution seismic data, which were previously published by Nasıf et al. (2019), Vardar et al. (2018), Alp et al. (2018). This map can be able to show only the main morphological structures such as valley in Büyükçekmece Bay according to the coarse resolution due to wide spaces between seismic profiles.

    A sub bottom profiler (SBP) acoustic dataset to supplement the SSS dataset and identify deformations in the study area was also used. The SBP provides continuous high-resolution seismic images of the upper sedimentary layer from the seafloor to an average depth of 30 m and is widely used as one of the main methods in high resolution seafloor surveys (Nasıf et al., 2019). The SBP used in this study was obtained using the BATHY 2010P engineering seismic system, which generates CHIRP signals in the 275−675 kHz band range. Position information was recorded simultaneously with the Magellan Proflex 500 scientific GPS on the header of the data via the seismic system. The tolerance of the system, which receives the position information from 20 satellites simultaneously, is ± 1 m. The obtained data with odc extension were converted to SEG-Y format in the system’s own program, filtering and amplitude gain were applied to the data using the kogeo seismic toolkit (v. 2.7). Time (ms)-depth (m) conversions were made using 1 500 m/s for seawater and near-surface sediments (Aksu et al., 2016).

    Approximately 250 km of side-scan sonar data and three seismic profiles were collected in the study area (Fig. 3). The reflection intensity (Fig. 2), acoustic returns (Table 1), and spatial distributions of acoustic data at the southern shelf of Istanbul (between Küçükçekmece-Büyükçekmece lagoons) allowed mapping of natural formations, civil engineering structures, and the deformations and morphological formations from port activities.

    Figure  3.  The location map of the acoustic data (side scan sonar, and sub bottom profiler), and the mosaic map.

    Gravel and mass transport deposition units are prevelant whole study area and determined at 0−2 m water depths. Sand reflections were generally recognized between 0−5 m in the water depths at near coastal areas of Büyükçekmece Bay, between Ambarlı harbor and Gürpınar fishing port, between Ambarlı harbor and Avcılar fishing port and nearshore of the Küçükçekmece Lagoon. However, the sandy units were distributed between 5−18 m water depths in Küçükçekmece Lagoon, the rest of the shallower areas were covered by benthic habitats possibly connected to sunlight up to a depth of 5 m.

    Towards from Büyükçekmece bay to the Gürpınar fishing port, at 5−10 m water depths, the reflection of the sandy mud unit is dominant and covered approximately 0.5 km to 1 km spatial area from the shore. This formation is getting narrower from west to east in accordance with the sea-bottom morphology. The muddy sand unit reflection that extends to Küçükçekmece offshore, covers the area up to the 20 m water depth and sandy mud unit reflections are determined in the areas deeper than 20m. Sandy Mud formation was dominantly observed at the center Büyükçekmece bay, in an area of approximately 10 km2. Mud formation was observed predominantly in Büyükçekmece bay and Gürpınar-Küçükçekmece (after about 1 km). Terrestrial debris flows (Fig. 4) were also observed along the entire coast. A small sea-floor deformation is observed on the riverfront near Gürpınar/Büyükçekmece (Fig. 5). In the east of Gürpınar fishing port, it has observed a possibly active sandbank structure, which is 100 m long, 10 m wide with a height of 0.5 m.

    Figure  4.  Side scan sonar (SSS) ecograms showing the difference acoustic reflections.
    Figure  5.  Morphological structures formed on the seafloor.

    Artificial coastal structures constructed by humans and related acoustic impact reflections on the seafloor are given in Figs 6-8. The study area is highly used for ship transportation and fishing because of westmarine marina, Ambarlı Port, fishing ports; therefore, ship traffic is highly intense and related sea-floor deformations are observed in the acoustic data. Especially offshore and nearby seafloor areas of Ambarlı Port are suffered from anchor damages that can be clearly observed as a linear line deformation. The anchor deformations observed generally show an area of about 5 km2 in front of the Ambarlı Port and in an area of 2 km2 in front of Küçükçekmece Lagoon (between 250−1 000 m water depths). There are also random anchor deformations determined in Avcılar, Gürpınar and Büyükçekmece bays (Fig. 6). In addition, the same directional deformation reflections, which consist of two parallel deformation planes and with parallel cuts in themselves, were encountered. These structures seem to consist of the impact of two elements at certain intervals on the seafloor. Due to this formation mechanism of the reflection, the possibility of trawling fishing in this area has been revealed.

    Figure  6.  Deformations caused by fishing and the boats on the seafloor (anchor and trawl web tracks).
    Figure  7.  Port and supply line feet view.
    Figure  8.  Pipelines, wreck, and rubble flow images.

    In places, the sedimentary units such as muds are randomly deformed as cut shortly or fluctuated from the sediment type. This reflection feature is generally observed at the near the ports and approximations at 0−5 m water depths and considered as the source of the pitch effect on the water loop and related distribution effect on the mobilization of the seafloor sediments. Seafloor interactions with engineering structures constructed in nearby coastal areas (such as port feet, pipelines, fuel platforms) and deformation effects such as scraping the bottom while these structures were made, in addition, the submarine morphological elements (Fig. 7) were determined that can be formed and evolved due to the change of the hydrographic system. Traces of the engineering structures, effects of the ships and fishermen, deformations of the wastewater discharge, pipeline passages (natural gas, water, etc.), rubbles, etc., and shipwrecks are also strongly affecting the study area (Fig. 8) 30 m long and 7 m wide, reflection interpreted as a wreck is determined at the west of the Gürpınar.

    In the seismic data obtained in the study area, formations of sediment types, outcrops, reefs, paleoshorelines, etc. on the seafloor were displayed according to reflection types (Fig. 9). Paleoshorelines are determined according to the reflection types and sediment truncations on the seismic profiles that indicate the sea level still stands. These levels are indicated as wave-cut terraces at Alp et al. (2018). These areas are in the S-N direction in Büyükçekmece bay (Fig. 9) and Avcılar offshore.

    Figure  9.  Seafloor natural structures and formation types by seismic method (SBP Line 1) (a); paleo shoreline, gas, and formation types (SBP Line 2) (b); formation types, rock exposure and pipeline view (SBP Line 3) (c).

    The deformations and the different reflections of the sediments can be clearly identified from the SSS and SBP data (Figs 4-9). However, it is hard to say the sediment type according to only the reflections. Even if the reflection types are similar (Barnhardt et al., 1998), the reflection intensity values are different from other studies (Grindlay, 2009; Collier and Brown, 2005). It is clear that the grounding of the reflections should be done with sampling methods or maybe video captures. So, correlations with the sediment distribution maps previously given (Oktay, 1998; Olgun, 2001; Alpar et al., 2014) were made in this study.

    It is observed that “Mud (M), Sand (S), sandy Mud (sM), muddy Sand (mS), Sandy Silt, Silty Sand” unit groups are dominant in the region. There are also debris flows from terrestrial inputs along the coastline. SM type represent the most dominant sediment group in the region. This group is generally distributed in low slope deepening control and in areas deeper than 25 m in accordance with shelf morphology. It is also widely recognized in the Büyükçekmece valley. Sea-bottom topography, regional flow system and possible detritial intense input are main control effects of the sediment distribution. Relatively parallel sediment type distributions (Fig. 10) indicate that the longshore currents are dominant in the study area and play an important role in sediment distributions. This finding is relatively different from the mean sea level circulations given in Chiggiato et al. (2012).

    Figure  10.  Seafloor sediment distributions and deformation map.

    Also, climate changes, waves and seafloor morphologies play decisive roles with current on sediment transportation, deposition, and erosion of the sediments with in general. According to local conditions, waves and streams erode the rocks in the coastal areas and cause coastal progression or sediment accumulation. Sediment reaches a dynamic balance in terms of mobilization. This process is due to thousands of years of influence from external factors such as wind, waves and currents and sources such as streams that feed them and eventually lead to material loss from them. When the balance occurs between these factors, both a stable shoreline and a stable sea bottom profile will emerge; no significant erosion (coastal regression) or accumulation (coastal progression) is encountered.

    The presence sediments of the Büyükçekmece bay have different characteristics at the interior and nearshore. It can also be possible with these sediments originating from the coastal landslide, the tectonic movements the region has experienced from time to time and the longshore current system in the region (Yaltirak, 2002; Derman, 2004). The wide part of the seafloor between Büyükçekmece and Küçükçekmece lagoons are covered with the mud-dominant (M) sediments (Altinok et al., 2009). This may represent more stable and stagnant conditions for the longshore current system. This deposition character is also against Chiggiato et al. (2012). That shows the general surface circulation of the Sea of Marmara is not controlling the sediment distributions of the study area, which probably has unique deep circulations (Özgan, 2020).

    The dominant material deposits that can be associated with landslide debris are prominently observed close to the shore in the Gürpınar region. The bottom current regime of the region prevents material accumulation between Büyükçekmece and Küçükçekmece, and the bottom flows of the Bosporus limit the sediment transportation to the region due to the location of the bathymetric threshold at the front of Yeşilköy-Bakırköy. Dark and wide reflections are interpreted as topographical sea continuity of the coastal morphology. The sediment transport from Küçükçekmece Lagoon to the marine can be observed. The Küçükçekmece Lagoon floor consists of sediments with high cohesive and adsorption capacities (Algan, 1987), except for the southern part, which consists of a sandy bottom material. It is explained that the base material consists of coarse-grained sediments in the connection areas of the Küçükçekmece Lagoon compared to other regions, and the coarse-grained material is transported from the shore to the lagoon by the currents and winds entering the connection channel (Algan, 1987).

    Port activities have heavily damaged the seafloor of the study area. These damages can be observed as: anchor deformation and associated floor dredging, destructive traces of the trawl fishing net, engineering structures built on the near shore and seafloor (such as natural gas pipelines, fishing ports, marinas, and harbor piles) and associated shallowing according to the sedimentary deposition. The constructions affect marine species, which pose a serious danger to the seas. The most important factors that disrupt the balance of the coastal profile is the uncontrolled material drainage from the coasts and shores of the coast and the materials that feed the shore, such as dams and unconscious structuring. Erosion or shallowness, carvings or spurs from sea structures such as harbors, shelters, coastal walls and breakwaters are the best-known examples. Depending on all these, sediment transport changes along the coast and perpendicular to the coast and erosion and/or accumulation occur on the coasts. In this context, Sarı et al. (2013, 2014) draws attention to the presence of anthropogenic pollutants in the study area and indirectly supports the findings of human origin in the region.

    This study mainly focuses on presenting the acoustic identification of the sea-floor sediment classification of the nearshore zone and the deformations caused by engineering structures and human-sourced impacts between Küçükçekmece–Büyükçekmece lagoons. Human-induced deformations and/or depositional conditions according to the intensive usage of the study area are presented in this study.

    The distribution of the sediment reflections is highly heterogeneous in the study area, waves, hydrodynamic conditions, the amount of material carried from the land, and the variable bathymetry are the important factors on the accumulation and deposition of the sedimentary units. Structures built on the shore, in particular, affect the carrier properties of current systems and cause the formation of dune structures in their vicinity. These dunes are considered to be still active and will therefore become shallower in the near future, creating a barrier to marine traffic. This event reveals the importance of conducting detailed hydrographic and oceanographic research before these structures are built. It shows that the construction of such structures should be avoided, especially in areas where foreshore currents are dominant. In addition, erosion systems are active in those areas, likely preventing these dunes from being stored where they would normally be transported. As a result, a previously existing beach area may have vanished. Although this idea cannot be proven since there is no map showing the recent past in the region, it reveals how important the mapping of marine areas is. In this respect, this study will be an important reference and source of discussion for future studies.

    Comparing the conventional methods, the study area can be imaged with wider swath, however, still gaps on the reflection map. Therefore, the sediment distribution map previously given in (Oktay, 1998, Alpar et al., 2014) was modified by overlying with SSS data and the re-draw manually. Thus, the weaknesses of the two methods were avoided, and maps that were more accurate could be obtained.

    Acknowledgements: The authors gratefully acknowledge that the marine researches and data collections of this study were supported by “Batı İstanbul Eğitim Araştırma ve Dalış Merkezi (West Istanbul Education Research and Diving Center)”.
  • Anderson L W J. 2005. California’s reaction to Caulerpa taxifolia: a model for invasive species rapid response. Biological Invasions, 7(6): 1003–1016. doi: 10.1007/s10530-004-3123-z
    Bischof K, Hanelt D, Wiencke C. 2000. Effects of ultraviolet radiation on photosynthesis and related enzyme reactions of marine macroalgae. Planta, 211(4): 555–562. doi: 10.1007/s004250000313
    Cai Yixun. 2021. Effect of environmental factors on growth, physiological and biochemical characteristics of Caulerpa lentillifera (in Chinese)[dissertation]. Guangzhou: South China University of Technology
    Carruthers T J B, Walker D I, Huisman J M. 1993. Culture studies on two morphological types of Caulerpa (Chlorophyta) from Perth, Western Australia, with a description of a new species. Botanica Marina, 36(6): 589–596
    Chaves Filho G P, Batista L A N C, de Medeiros S R B, et al. 2022. Sulfated glucan from the green seaweed Caulerpa sertularioides inhibits adipogenesis through suppression of adipogenic and lipogenic key factors. Marine Drugs, 20(8): 470. doi: 10.3390/md20080470
    da Silva L P, Pereira E, Prieto M A, et al. 2019. Rubus ulmifolius Schott as a novel source of food colorant: extraction optimization of coloring pigments and incorporation in a bakery product. Molecules, 24(11): 2181. doi: 10.3390/molecules24112181
    Davis A R, Roberts D E, Cummins S P. 1997. Rapid invasion of a sponge-dominated deep-reef by Caulerpa scalpelliformis (Chlorophyta) in Botany Bay, New South Wales. Austral Ecology, 22(2): 146–150. doi: 10.1111/j.1442-9993.1997.tb00653.x
    de Gaillande C, Payri C, Remoissenet G, et al. 2017. Caulerpa consumption, nutritional value and farming in the Indo-Pacific region. Journal of Applied Phycology, 29(5): 2249–2266. doi: 10.1007/s10811-016-0912-6
    Dennison W C. 1987. Effects of light on seagrass photosynthesis, growth and depth distribution. Aquatic Botany, 27(1): 15–26. doi: 10.1016/0304-3770(87)90083-0
    Ding Lanping, Huang Bingxin, Luan Rixiao. 2015. New classification system of marine green algae of China. Guangxi Sciences (in Chinese), 22(2): 201–210
    Ebadi S, Ashaari Z, Late Masoumi H, et al. 2019. Evaluation of bending strength of hydrothermally treated oil palm wood in various buffered media using response surface methodology. Journal of Tropical Forest Science, 31(2): 151–161. doi: 10.26525/jtfs2019.31.2.151161
    Faramarzi S, Anzabi Y, Jafarizadeh-Malmiri H. 2019. Selenium supplementation during fermentation with sugar beet molasses and Saccharomyces cerevisiae to increase bioethanol production. Green Processing and Synthesis, 8(1): 622–628. doi: 10.1515/gps-2019-0032
    Feng Lina, Shi Xiaoyong, Chen Yuehong, et al. 2021. Effects of temperature on the nitrate reductase activity and growth of Ulva prolifera. Journal of Phycology, 57(3): 955–966. doi: 10.1111/jpy.13141
    Fernández C, Cortés J. 2005. Caulerpa sertularioides, a green alga spreading aggressively over coral reef communities in Culebra Bay, North Pacific of Costa Rica. Coral Reefs, 24(1): 10. doi: 10.1007/s00338-004-0440-8
    Flexas J, Bota J, Loreto F, et al. 2004. Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biology, 6(3): 269–279. doi: 10.1055/s-2004-820867
    Gao Kunshan. 2014. Algal Carbon Fixation: Basis, Advances and Methods (in Chinese). Beijing: Science Press
    Gong Shusen, Yang Fei, Wang Qingfen, et al. 2022. Processing of Noni Liquor based on response surface methodology. PeerJ, 10: e13817. doi: 10.7717/peerj.13817
    Guo Hui, Yao Jianting, Sun Zhongmin, et al. 2015. Effects of salinity and nutrients on the growth and chlorophyll fluorescence of Caulerpa lentillifera. Chinese Journal of Oceanology and Limnology, 33(2): 410–418. doi: 10.1007/s00343-015-4105-y
    Hadiyat M A, Sopha B M, Wibowo B S. 2022. Response surface methodology using observational data: a systematic literature review. Applied Sciences, 12(20): 10663. doi: 10.3390/app122010663
    Huang Jianhui. 2012. Effects of concentrations of nitrogen and phosphorus and different culture methods on the growth of Caulerpa lentillifera. Journal of Fujian Fisheries (in Chinese), 34(5): 416–419
    Jiang Haiyan, Wu Sichao, Cen Yingzhou. 2011. Nutrient component analysis of six kinds of economic algae in Zhanjiang sea area. Guangzhou Chemical Industry (in Chinese), 39(7): 105–108
    Kang E J, Lee S, Kang J, et al. 2021. Performance of a potentially invasive species of ornamental seaweed Caulerpa sertularioides in acidifying and warming oceans. Journal of Marine Science and Engineering, 9(12): 1368. doi: 10.3390/jmse9121368
    Kim M, Lee B, Kim H S, et al. 2019. Increased biomass and lipid production of Ettlia sp. YC001 by optimized C and N sources in heterotrophic culture. Scientific Reports, 9(1): 6830. doi: 10.1038/s41598-019-43366-5
    Klein J C, Verlaque M. 2008. The Caulerpa racemosa invasion: a critical review. Marine Pollution Bulletin, 56(2): 205–225. doi: 10.1016/j.marpolbul.2007.09.043
    Kolar C S, Lodge D M. 2001. Progress in invasion biology: predicting invaders. Trends in Ecology & Evolution, 16(4): 199–204
    Kramar A, Turk S, Vrečer F. 2003. Statistical optimisation of diclofenac sustained release pellets coated with polymethacrylic films. International Journal of Pharmaceutics, 256(1–2): 43–52. doi: 10.1016/S0378-5173(03)00061-9
    Kumar M, Gupta V, Kumari P, et al. 2011. Assessment of nutrient composition and antioxidant potential of Caulerpaceae seaweeds. Journal of Food Composition and Analysis, 24(2): 270–278. doi: 10.1016/j.jfca.2010.07.007
    Landi S, Santini G, Vitale E, et al. 2022. Photosynthetic, molecular and ultrastructural characterization of toxic effects of zinc in Caulerpa racemosa indicate promising bioremediation potentiality. Plants, 11(21): 2868. doi: 10.3390/plants11212868
    Lapointe B E, Barile P J, Wynne M J, et al. 2005. Reciprocal Caulerpa invasion: Mediterranean native Caulerpa ollivieri in the Bahamas supported by human nitrogen enrichment. Aquatic Invaders, 16(2): 2–5
    Li Tianjingwei, Ma Bin, Zou Xiaoxiao, et al. 2022. Physiological mechanism of response to temperature stress in seaweed Caulerpa lentillifera. Chinese Journal of Fisheries (in Chinese), 35(4): 67–73
    Liu Rui, Li Yongmei, Wang Yixiao, et al. 2019. Biogeographical distribution, biological characteristics and biological invasion of Caulerpa (Chlorophyta) seaweeds. Journal of Anhui Agricultural Sciences (in Chinese), 47(4): 95–98, 104
    Liu Hengtong, Wang Fang, Wang Qiaohan, et al. 2016. A comparative study of the nutrient uptake and growth capacities of seaweeds Caulerpa lentillifera and Gracilaria lichenoides. Journal of Applied Phycology, 28(5): 3083–3089. doi: 10.1007/s10811-016-0858-8
    Mäkelä M. 2017. Experimental design and response surface methodology in energy applications: a tutorial review. Energy Conversion and Management, 151: 630–640. doi: 10.1016/j.enconman.2017.09.021
    Mee R W. 2009. A Comprehensive Guide to Factorial Two-Level Experimentation. New York: Springer
    Meinesz A, Belsher T, Thibaut T, et al. 2001. The introduced green alga Caulerpa Taxifolia continues to spread in the mediterranean. Biological Invasions, 3(2): 201–210. doi: 10.1023/A:1014549500678
    Nazzal S, Nutan M, Palamakula A, et al. 2002. Optimization of a self-nanoemulsified tablet dosage form of ubiquinone using response surface methodology: effect of formulation ingredients. International Journal of Pharmaceutics, 240(1–2): 103–114. doi: 10.1016/S0378-5173(02)00130-8
    Nur M M A, Garcia G M, Boelen P, et al. 2019. Enhancement of C-phycocyanin productivity by Arthrospira platensis when growing on palm oil mill effluent in a two-stage semi-continuous cultivation mode. Journal of Applied Phycology, 31(5): 2855–2867. doi: 10.1007/s10811-019-01806-9
    Okur N, Çengel M, Göçmez S. 2002. Influence of salinity on microbial respiration and enzyme activity of soils. Acta Horticulturae, (573): 189–194
    Pang Meixia, Huang Zhili, Liu Xiaolong, et al. 2021. Effects of heavy metal cadmium on Caulerpa lentillifera based on transcriptome analysis. Chinese Journal of Applied Ecology (in Chinese), 32(12): 4447–4456
    Piazzi L, Ceccherelli G, Cinelli F. 2001. Threat to macroalgal diversity: effects of the introduced green alga Caulerpa racemosa in the Mediterranean. Marine Ecology Progress Series, 210: 149–159. doi: 10.3354/meps210149
    Piazzi L, Cinelli F. 1999. Développement et dynamique saisonnière d'un peuplement méditerranéen de l′algue tropicale Caulerpa racemosa (Forsskl) J. Agardh. Cryptogamie Algologie, 20(4): 295–300. doi: 10.1016/S0181-1568(00)88146-5
    Pinheiro A M, Maia G A, Figueiredo R W, et al. 2022. Response surface methodology optimization of blended fruit nectar: cashew apple and açai. International Journal of Fruit Science, 22(1): 275–286. doi: 10.1080/15538362.2022.2037037
    Ruitton S, Verlaque M, Boudouresque C F. 2005. Seasonal changes of the introduced Caulerpa racemosa var. cylindracea (Caulerpales, Chlorophyta) at the northwest limit of its Mediterranean range. Aquatic Botany, 82(1): 55–70. doi: 10.1016/j.aquabot.2005.02.008
    Shevchenko N M, Burtseva Y V, Zvyagintseva T N, et al. 2009. Polysaccharides and sterols from green algae Caulerpa lentillifera and C. sertularioides. Chemistry of Natural Compounds, 45(1): 1–5. doi: 10.1007/s10600-009-9223-3
    Shi Jianhong. 2008. Field survey and culture studies of Caulerpa in Taiwan (in Chinese)[dissertation]. Taipei: National Sun Yat-Sen University
    Shi Xiaohan, Zou Dinghui, He Quan, et al. 2022. Photophysiological characteristics of the branch and stolon of macroalga Caulerpa lentillifera (Caulerpaceae, Caulerpa) under different growth light conditions, and their responses to temperature rise. Journal of Tropical Oceanography (in Chinese), 41(5): 150–160
    Smith T B, Fong P, Kennison R, et al. 2010. Spatial refuges and associational defenses promote harmful blooms of the alga Caulerpa sertularioides onto coral reefs. Oecologia, 164(4): 1039–1048. doi: 10.1007/s00442-010-1698-x
    Smith C M, Walters L J. 1999. Fragmentation as a strategy for Caulerpa species: fates of fragments and implications for management of an invasive weed. Marine Ecology, 20(3–4): 307–319. doi: 10.1046/j.1439-0485.1999.2034079.x
    Srinivas G, Nidoni U, Ramachandra C T, et al. 2019. Supercritical fluid extraction of pupae oil from mulberry silkworm (Bombyx mori L.). Journal of Pharmacognosy and Phytochemistry, 8(3): 4507–4513
    Stensrud G, Sande S A, Kristensen S, et al. 2000. Formulation and characterisation of primaquine loaded liposomes prepared by a pH gradient using experimental design. International Journal of Pharmaceutics, 198(2): 213–228. doi: 10.1016/S0378-5173(00)00338-0
    Stuthmann L E, Springer K, Kunzmann A. 2021. Cultured and packed sea grapes (Caulerpa lentillifera): effect of different irradiances on photosynthesis. Journal of Applied Phycology, 33(2): 1125–1136. doi: 10.1007/s10811-020-02322-x
    Tong Yanmei, Chen Xiuli, Hu Tingjun, et al. 2022. Optimization of extraction process and antioxidant activity of polysaccharides from Caulerpa lentillifera by response surface methodology. Journal of Fisheries of China (in Chinese). https://kns.cnki.net/kcms/detail/31.1283.S.20220518.1019.004.html[2022-05-18/2022-12-20]
    Verlaque M, Afonso-Carrillo J, Gil-Rodríguez M C, et al. 2004. Blitzkrieg in a marine invasion: Caulerpa racemosa var. cylindracea (Bryopsidales, Chlorophyta) reaches the Canary Islands (north-east Atlantic). Biological Invasions, 6(3): 269–281. doi: 10.1023/B:BINV.0000034589.18347.d3
    Vishwakarma R, Banerjee R. 2019. Process optimization for enhancement of fermentable sugar from Cyperus sp. through enzymatic saccharification. Journal of Biofuels, 10(1): 1–11
    Wang Zewen. 2010. Study on the determination of seaweed growth regulator and fertilizer efficiency (in Chinese)[dissertation]. Qingdao: Ocean University of China
    Wang Zhan. 2015. Preliminary studies on environmental adaptation and paling mechanism of Caulerpa (in Chinese)[dissertation]. Shantou: Shantou University
    Wang Zonghua, Sun Na, He Yao, et al. 2014. DNA assembled gold nanoparticles polymeric network blocks modular highly sensitive electrochemical biosensors for protein kinase activity analysis and inhibition. Analytical Chemistry, 86(12): 6153–6159. doi: 10.1021/ac501375s
    Wells C M, Di Cera E. 1992. Thrombin is a sodium ion activated enzyme. Biochemistry, 31(47): 11721–11730. doi: 10.1021/bi00162a008
    Williams S L. 1984. Uptake of sediment ammonium and translocation in a marine green macroalga Caulerpa cupressoides. Limnology and Oceanography, 29(2): 374–379. doi: 10.4319/lo.1984.29.2.0374
    Williams S L, Schroeder S L. 2004. Eradication of the invasive seaweed Caulerpa taxifolia by chlorine bleach. Marine Ecology Progress Series, 272: 69–76. doi: 10.3354/meps272069
    Withgott J. 2002. California tries to rub out the monster of the lagoon. Science, 295(5563): 2201–2202. doi: 10.1126/science.295.5563.2201
    Xu Ning, Duan Shunshan, Li Aifen, et al. 2010. Effects of temperature, salinity and irradiance on the growth of the harmful dinoflagellate Prorocentrum donghaiense Lu. Harmful Algae, 9(1): 13–17. doi: 10.1016/j.hal.2009.06.002
    Yu Ping. 2005. Effect of temperature, irradiance and population interaction on the growth of phytoplankton of East China Sea (in Chinese)[dissertation]. Qingdao: Ocean University of China
    Zhang Meijian, Ma Yurong, Che Xinyi, et al. 2020. Comparative analysis of nutrient composition of Caulerpa lentillifera from different regions. Journal of Ocean University of China, 19(2): 439–445. doi: 10.1007/s11802-020-4222-x
    Zhao Yuping, Chen Xiaowang, Shen Pengwei. 2013. Optimization of culture medium to produce manganese peroxidase by using Box-Behnken experimental design and response surface methodology. Science and Technology of Food Industry (in Chinese), 34(4): 207–211
    Zhong Yiyun, Yang Yunqi, Gao Xiaofeng, et al. 2021. Effects of salinity, temperature and light intensity on growth and photosynthetic activity of Caulerpa sertularioides. Journal of Tropical and Subtropical Botany (in Chinese), 29(6): 626–633
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