Spatiotemporal distribution patterns of macrobenthic communities and their relationship with environmental factors in the Shengsi Archipelago (Zhejiang, China)
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Abstract: Macrobenthic organisms are commonly employed as biomonitors for environmental risk assessment. In this study, we aimed to investigate the spatial and temporal patterns of the macrobenthic community, which is influenced by environmental factors of sediments and bottom water layer. We sampled a total of 12, 11, 10, and 11 stations in the Shengsi Archipelago during June 2010, August 2010, November 2020, and April 2021 respectively. A total of 124 species of macrobenthos were identified, with polychaetes being the dominant group. The abundance, biomass, and diversity indices exhibited no significant temporal differences. Similarly, biodiversity did not exhibit a clear spatial gradient, likely due to the small study area and the absence of significant differences in key factors such as depth. However, the stations with the lowest biodiversity values consistently appeared in the southwest region, possibly due to the impact of human activities. Significant differences in the macrobenthic community were observed between all months except between June and August, and mollusk Endopleura lubrica and polychaete Sigambra hanaokai were important contributors to these differences according to the results of the Similarity Percentages analysis. Suspended particulate matter (SPM) was identified as the primary driving factors of macrobenthic variability. In summary, the community structure underwent temporal changes influenced by complex current patterns, while biodiversity remained relatively stable. This study contributes to our understanding of the key environmental factors affecting macrobenthic communities and biodiversity. It also provides valuable data support for the long-term monitoring of macrobenthos and the environment in the Shengsi Archipelago.
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1. Introduction
In recent years, biological invasions have gradually become the greatest threat to ecosystems. Codium is a group of large, multinucleate, tubular green algae with an intertidal or subtidal distribution in the tropics and subtropics (Silva, 1955). Some species of this genus are recognized as one of the greatest threats to shallow water ecosystems due to their proliferation as invasive seaweeds (Vitousek et al., 1957), such as Codium fragile, which encroach on the habitat of other organisms (Drouin et al., 2012).
On the other hand, Codium is also an important genus of seaweed resources. The extract of C. tomentosum can be used as the raw material of cosmetics (Wang et al., 2015; Leandro et al., 2020). Extract of C. cylindricum can act as an anticoagulant and antioxidant (Matsubara et al., 2001; Yan et al., 2021). Codium fragile has the effect of expelling parasites from the human body, and its extract also has antitumor, antibacterial, and anticoagulant effects (Yin et al., 2007; Ye et al., 2010; Wei and Zheng, 2021). Therefore, research on the physiological characteristics of Codium is important for both biological invasion control and seaweed resource development.
How Codium can invade successfully has attracted the attention of several scholars. Contrary to popular belief, some species of this genus can be attached to soft substrates rather than only to hard substrates (Williams, 2007). In addition, their broad physiological tolerance and high growth rate in summer and early autumn are also conducive to their widespread expansion (Yang et al., 1997; Malinowski and Ramus, 1973; Hanisak, 1979; Benson et al., 1983; Hanisak and Harlin, 1978). Hanisak (1979) systematically studied the effects of temperature, light, salinity, and nitrogen source on the growth of C. fragile in combination with field experiments and indoor culture, and found that the growth pattern of C. fragile in the field was mainly affected by temperature and light intensity. Marques et al. (2022) considered light availability as a major parameter affecting the growth of macroalgae.
However, there are few studies on the physiological and biochemical responses of Codium species to the above environmental factors. Some scholars believe that light is the main factor affecting the growth of macroalgae such as Codium (Marques et al., 2022; Magnusson et al., 2015), and light also regulates the effects of other environmental stressors on the photosynthetic performance of algae (Gao et al., 2016, 2018). To investigate the relationship between the invasiveness of Codium species and their photo-adaptation, two species C. fragile and C. cylindricum were selected as experimental samples for a comparative study. Codium fragile is native to Japan and has now invaded several regions around the world, including the northwest Atlantic coast, the U.S. State of Florida, southern New England, the Mediterranean Sea, Australia, New Zealand, and Chile, mainly in the intertidal zone (Silva, 1955; Israel et al., 2010; Trowbridge, 1995; Bird et al., 1993; Carlton and Scanlon, 1985; Chapman, 1998; Neill et al., 2006; Churchill and Moeller, 1972; Pérez-Cirera et al., 1989; Lapointe et al., 2005; Dromgoole, 1975; Ding et al., 2022). According to the data from AlgaeBase, C. cylindricum, which was also first recorded in Japan, is now mainly distributed in Japan, Korea, the South China Sea, and coastal areas of Southeast Asia, growing mostly in the lower intertidal to subtidal areas. In this study, the chlorophyll fluorescence analysis technique was used to indirectly measure the changes in their photosynthesis and to examine their photosynthetic physiological responses to different light intensities. The pigment content, malondialdehyde content, peroxidase activity, and total antioxidant capacity (T-AOC) were also measured for the investigation of their physiological and biochemical responses to different light intensities. The invasive photo-adaptation strategies of C. fragile were inferred and generalized based on comparing the differences among photosynthetic physiological, physiological, and biochemical responses of the two species of Codium to different light intensities.
2. Materials and methods
2.1 Materials preparation
The mature spongiform thalli of C. fragile and C. cylindrical were collected from the Shen’ao Bay, Nan’ao Island, China in March 2011. The epiphytes and protozoa on the surface of the specimen were removed with paintbrushes, and the specimens were rinsed several times with sterile seawater and checked under the dissecting microscope (Olympus LG-PS 2, Japan). The thalli were divided into several parts and were cultured in
1000 mL clear plastic bottles containing sterile natural seawater (salinity of 30).2.2 Laboratory culture
The thalli were cultured in 20℃ climate-controlled culture chambers (GXZ-380 B, China) and were illuminated by daylight-type, white fluorescent tubes, photoperiod 12:12 (L:D). Five tiers of illuminance were designed, which were 10, 30, 60, 90, and 120 μmol/(m2∙s). To reduce the effects of pollution, the medium was replaced every day.
2.3 Rapid light curve (RLC) analysis
The optimal photochemical efficiency of photosynthesis (Fv/Fm) and rapid light curve (RLC) were measured with an imaging-PAM fluorometer (PAM-Water-ED, Walz, Germany). The samples were exposed to successive light intensity (calculated by photons) gradients (PAR 0, 21, 56, 55, 111, 186, 281, 336, 396, 461, 531 μmol/(m2∙s)) for 10 s each step. The relative electron transfer rate (rETR) and the effective quantum yield of PSII were calculated simultaneously at each light intensity according to the following equation (Schreiber, 2004):
$$ \left.\begin{array}{l} \mathrm{rETR=} {Y} \mathrm{(II)}\times PAR\times 0.84\times 0.5\\ {Y} \mathrm{(II)} =({F}'_{ \mathrm{m}} - {F} _{ \mathrm{s}} )/ {F}^\prime _{ \mathrm{m}} \end{array}\right\} $$ (1) where Y(II) is the efficient quantum yield of photosystem II, F'm is the light-adapted maximum fluorescence and Fs is the light-adapted steady-state fluorescence. Rapid light curves were fitted according to the following equation (Platt et al., 1980):
$$ {P} = {P}_{ \mathrm{m}} ({1-e}^{ -{\alpha } \times \mathrm{PAR/} {P}_\mathrm{m}} ) {e}^{ - {\beta } \times \mathrm{PAR/} {P}_\mathrm{m}} , $$ (2) where P is the photosynthetic rate or relative electron transfer rate, Pm is the maximum relative electron transfer rate (rETRmax), α is the photosynthetic rate in the light-limited region of RLC, and β is the photoinhibition parameter.
In addition, the minimum saturating irradiance (Ek) was calculated according to the following equation (Bouman et al., 2018):
$$ \mathit{E} _{ \mathrm{k}} \mathrm= \mathit{P} _{ \mathrm{m}} \mathrm{/} \mathit{\alpha } \mathrm{.} $$ (3) 2.4 Chlorophyll fluorescence quenching analysis
The photochemical quenching (qP) and non-photochemical quenching (NPQ) coefficients of chlorophyll fluorescence are calculated based on the internal function of Imaging-PAM with the following equation (Guidi and Degl’Innocenti, 2012):
$$ \left. \begin{array}{l}\mathrm{qP} =( {F}'_{\mathrm{m}} - {F} _{ \mathrm{t}} )/ ( {F}' _{ \mathrm{m}} - {F} _{ \mathrm{0}} )\\ \mathrm{NPQ} =( {F} _{ \mathrm{m}} - {F}'_{ \mathrm{m}} / {F}'_{ \mathrm{m}} \end{array}\right\} $$ (4) 2.5 Photosynthetic pigments measurement
After 7 d of culture, 0.1 g of thalli (FW) was weighed and extracted with 5 mL of 100% methanol. The extract was stored in a refrigerator at −4℃ for 24 h in the dark. Whereafter, the extract was centrifuged at 5 000× g and 4℃ for 10 min. The absorbance of the extract was measured with an ultraviolet-visible spectrophotometer (Shimadzu, UV-2450, Japan) and the control group was methanol. The content of chlorophyll a (Chl a) and carotenoids (Car) was calculated according to the following equation (Porra, 2002; Parsons and Strickland, 1963):
$$ \left.\begin{array}{l} {[\mathrm{Chl}\ a]} =16.29 \times A_{665}-8.54 \times A_{652} \\ {[\mathrm{Car}]} =7.6 \times\left(A_{480}-1.49 \times A_{510}\right) \end{array}\right\} $$ (5) 2.6 Malondialdehyde measurement
A total of 0.2 g of thalli (FW) that was cultured for 7 d was weighed and cut into pieces, and 2 mL of 10% TCA and a small amount of quartz sand were mixed with the pieces of thalli. The mixture was ground until homogenized. Then 2 mL of 10% TCA was added for further grinding, and the homogenate was centrifuged at 4 000 r/min for 10 min. The supernatant was the sample extract. A total of 2 mL of supernatant was aspirated (2 mL of distilled water for the control) and mixed with 2 mL of 0.6% TBA solution. The test tubes containing the mixture were boiled for 10 min (timed from the appearance of small bubbles in the solution in the test tubes). The tubes were then cooled, and centrifuged at 3 000 r/min for 15 min. The supernatant was collected and the absorbance values at 532 nm, 600 nm, and 450 nm were measured (the control group was used as a blank control). The concentration (cMDA, µmol/L) of malondialdehyde (MDA) was calculated according to the following equation:
$$ {c} _{ \mathrm{MDA}} = 6.45 ( {A}_{{532}} - {A}_{600} )-0.56 {A} _{450} $$ (6) where A450, A532, and A600 denote the absorbance values at 450 nm, 532 nm, and 600 nm, respectively. The content of MDA (CMDA, μmol/g) was then calculated using the following equation:
$$ \mathit{C} _{ \mathrm{MDA}} \mathrm{=(} \mathit{c} _{ \mathrm{MDA}} \mathit{V} _{ \mathrm{T}} \mathit{V} _{ \mathrm{1}} \mathrm{)/(1000} \mathit{V} _{ \mathrm{2}} \mathit{W} \mathrm{),} $$ (7) where VT is the total volume of the extract, Vl is the total volume of the extract and TBA solution reacted, V2 is the volume of the extract reacted with TBA, and W is the mass of the fresh sample.
2.7 Peroxidase activity measurement
After 7 d of culture, 0.2 g of thalli was weighed and mixed with 5 mL of 20 mmol/L KH2PO4. The mixture was ground into a homogenate in a mortar, centrifuged at 4 000 r/min for 15 min, and the supernatant was collected and stored in a cold place. The residue was extracted once more with 5 mL of KH2PO4 solution, and the supernatant of both times was combined. Take 2 colorimetric cups with an optical diameter of 1 cm. Add 3 mL of reaction mixture and 1 mL of KH2PO4 to one of the cups as a zero control, and add 3 mL of reaction mixture and l mL of enzyme solution to the other cup. The stopwatch was then turned on immediately and the OD value was measured at 470 nm in the spectrophotometer for 5 min, with readings taken at 1 min intervals. A curve was then made of the value of the change in OD with reaction time, and the slope of the initial linear portion of the curve was calculated as the value of the change in OD, i.e., ∆A470, expressed in [min·mg protein (or fresh weight g)].
2.8 Total antioxidant capacity (T-AOC) measurement
The total antioxidant capacity (T-AOC) of thalli was determined according to the instructions of the total antioxidant capacity assay kit of Nanjing Jiancheng Bioengineering Institute. The sample was weighed accurately and added 5 times the volume of phosphate-buffered saline (PBS) pH 7.0 at the ratio of weight (g): volume (mL) = 1:5, and the homogenate was prepared in an ice-water bath, centrifuged at 2 500 r/min for 10 min, and the supernatant was collected for measurement. The operation is according to Table 1.
Table 1. Operational procedure for the determination of T-AOCMeasurement tube Control tube Reagent 1/mL 1 1 Sample to be tested/mL a* Reagent 2/mL 2 2 Reagent 3/mL 0.5 0.5 Mix thoroughly with a vortex mixer, 37℃ water bath for 30 min Reagent 4/mL 0.2 0.2 Sample to be tested/mL a* Reagent 5/mL 0.2 0.2 Note: The reference sampling volume for 10% tissue homogenate is 0.2 mL. | Show Table
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Mix the reaction solution well and leave at 25−37℃ for 10 min. Set the spectrophotometer at 520 nm, 1 cm optical diameter, zero with double-distilled water, and measure the absorbance value of each tube.
The total antioxidant capacity was defined as one unit of total antioxidant capacity for every 0.01 increase in the absorbance (OD) of the reaction system per minute per gram of fresh weight thalli at 37℃. The total antioxidant capacity (T-AOC) was calculated according to the following equation:
$$ \mathrm{T-AOC}=\left[\left(\mathrm{OD}_{\mathrm{m}}-\mathrm{OD}_{\mathrm{c}}\right) / 0.01\right] \div 30 \times\left(V_{\mathrm{f}} / V_{\mathrm{s}}\right) \div \mathrm{FW} $$ (8) Where ODm is the OD of the sample, ODc is the OD of control, Vr is the total volume of the reaction solution, Vs is the volume of the sample and FW is the fresh weight (g) of the sample.
2.9 Statistical analysis
The rapid light curves were linearly fitted using SPSS 20. The data were processed using GraphPad Prism 5.0 and Excel. Significant differences between treatments were analyzed by one-way ANOVA or T-test, and the significance level was set at P<0.05.
3. Results
3.1 Effect of light on photosynthetic physiology of C. fragile and C. cylindricum
In the light intensity range of 10−120 μmol/(m2∙s), the optimal photochemical efficiency of photosynthesis (Fv/Fm) of C. fragile showed a decreasing trend, and the low light intensity group (10−30 μmol/(m2∙s)) had higher photosynthetic efficiency than the high light intensity group (60−120 μmol/(m2∙s)), and there was a significant difference. Whereas, the rapid light curves (RLCs) showed that the relative electron transfer rate (rETR) of the thalli was the lowest at low light intensities (10 μmol/(m2∙s)). The convexity of the rapid light curve (RLC) was the highest at a light intensity of 90 μmol/(m2∙s), and there was no sign of a decrease in the rETR with the increase in light intensity. The rETRmax showed a trend of rising and then decreasing. It reached a maximum at a light intensity of 90 μmol/(m2∙s). The initial slope of the rapid light curve (α) tended to rise and then fall, and the α value was maximum at a light intensity of 30 μmol/(m2∙s) and was significantly different from that of the high light intensity group. The minimum saturating irradiance (Ek) showed a rising and then decreasing trend, and increased significantly at 90 μmol/(m2∙s) (Figs 1−3).
Figure 1. The Fv/Fm of two Codium species cultured at different light intensities. a. The Fv/Fm of C. fragile cultured at different light intensities, and b. the Fv/Fm of C. cylindricum cultured at different light intensities. Different letters (a, b, c, and d) represent significant differences among groups.
Figure 2. The comparison of the RLCs of two Codium species cultured at different light intensities, a. The comparison of RLCs of C. fragile cultured at different light intensities, and b. the comparison of RLCs of C. cylindricum cultured at different light intensities.
Figure 3. The rETRmax, photosynthetic rate in the light-limited region of RLC (α), and Ek of two Codium species cultured at different light intensities. The data were obtained from RLCs. a. The comparison of rETRmax of C. fragile cultured at different light intensities, b. the comparison of rETRmax of C. cylindricum cultured at different light intensities, c. the comparison of α of C. fragile cultured at different light intensities, d. the comparison of α of C. cylindricum cultured at different light intensities, e. the comparison of Ek of C. fragile cultured at different light intensities, and f. the comparison of Ek of C. cylindricum cultured at different light intensities. Different letters (a, b, and c) represent significant differences among groups.The photochemical quenching curve (qP) was significantly lower in the lower light intensity range (10−60 μmol/(m2∙s)) than in the higher light intensity range (90−120 μmol/(m2∙s)), and the non-photochemical quenching curve (NPQ) of C. fragile was significantly higher at a light intensity of 120 μmol/(m2∙s) than the curves of other light groups, and the lowest NPQ was observed at a light intensity of 90 μmol/(m2∙s) (Figs 4 and 5).
Figure 4. The comparison of qP of two Codium species cultured at different light intensities. a. The comparison of qP of C. fragile cultured at different light intensities, and b. the comparison of qP of C. cylindricum cultured at different light intensities.
Figure 5. The comparison of NPQ of two Codium species cultured at different light intensities. a. The comparison of NPQ of C. fragile cultured at different light intensities, and b. the comparison of NPQ of C. cylindricum cultured at different light intensities.For C. cylindricum, the Fv/Fm tended to decrease in the light range of 10−120 μmol/(m2∙s), and the maximal photochemical efficiency was higher in the low light intensity group (10−30 μmol/(m2∙s)) than in the high light intensity group (90−120 μmol/(m2∙s)), with a significant difference. The RLCs showed that the rETR of the thalli was lowest at high light intensities (120 μmol/(m2∙s)), and the convexity of the RLC was higher than the other groups at a light intensity of 30 μmol/(m2∙s). The rETRmax tended to increase and then decrease and reached a maximum at a light intensity of 30 μmol/(m2∙s). The α tended to decrease gradually, and the α values of the low light intensity group (10−30 μmol/(m2∙s)) were significantly different from those of the high light intensity group (90−120 μmol/(m2∙s)). The Ek showed a gradual increase, and the Ek values in the low light intensity group (10−30 μmol/(m2∙s)) were significantly different from those in the high light intensity group (90−120 μmol/(m2∙s)) (Figs 1−3).
The qP was lower in the lower light intensity range (10−60 μmol/(m2∙s)) than in the higher light intensity range (90−120 μmol/(m2∙s)). The NPQ of C. cylindricum were significantly higher in the low light intensity group (10−30 μmol/(m2∙s)) than in the high light intensity group (90−120 μmol/(m2∙s)) (Figs 4 and 5).
3.2 Physiological and biochemical responses of spongiform thalli of C. fragile and C. cylindricum to different light intensities
Codium fragile was able to grow in the light intensity range of 10−120 μmol/(m2∙s) with no significant difference in chlorophyll content. Carotenoids showed an increasing trend in the light intensity range of 30−120 μmol/(m2∙s) (Fig. 6). The concentration of malondialdehyde (MDA) and peroxidase (POD) activity tended to increase with light enhancement, but there was no significant difference (Figs 7 and 8). The total antioxidant capacity (T-AOC) of thalli tended to increase and then decrease with the increase of light intensity, and the strongest total antioxidant capacity of thalli was found in the range of 60−90 μmol/(m2∙s) (Fig. 8).
Figure 6. The pigments contents of two Codium species under different light intensities. a. Contents of chloroplast, and b. contents of carotenoids. Letter a represent no significant differences among groups (p>0.05, ANOVA, followed by Tukey’s multiple comparison test).
Figure 7. The MDA contents of two Codium species under different light intensities. Different letters (a and b) represent significant differences among groups (p<0.05, ANOVA, followed by Tukey's multiple comparison test).
Figure 8. The comparison of POD activity (a, letters a represent no significant differences among groups (p>0.05, ANOVA, followed by Tukey's multiple comparison test)) and T-AOC (b, different letters (a and b) represent significant differences among groups (p<0.05, ANOVA, followed by Tukey's multiple comparison test)) of two Codium species under different light intensities.For C. cylindricum, it was able to grow in the light intensity range of 10−120 μmol/(m2∙s) with no significant difference in chlorophyll and carotenoids content (Fig. 6). In the range of 10−120 μmol/(m2∙s), the malondialdehyde (MDA) content of thalli showed a decreasing trend, and the highest malondialdehyde content of thalli was found at 10 μmol/(m2∙s) and significantly different from the high luminosity group (90 μmol/(m2∙s)) (Fig. 7). Peroxidase (POD) activity tended to increase with the enhancement of light (Fig. 8). And the total antioxidant capacity (T-AOC) increased first and then decreased with the enhancement of light. The total antioxidant capacity was strongest at the light intensity of 60 μmol/(m2∙s), which was significantly different from the low-light group (10 μmol/(m2∙s)) and high-light group (90−120 μmol/(m2∙s)), respectively (Fig. 8).
4. Discussion
The growth, reproduction, and chemical composition of seaweeds are influenced by the interaction of temperature, nutrients, and light (Marques et al., 2021). Therefore, the study of the combined effects of these factors on Codium is important for both invasion control and culture. Fv/Fm is the maximum photochemical quantum yield of PSII, reflecting the efficiency of light energy conversion within the PSII reaction center. The value varied little under non-stress conditions and was not affected by species and growth conditions, and it decreased significantly under stress conditions (Xu et al., 1992). In the light intensity range of 10−120 μmol/(m2∙s) in this paper, the Fv/Fm of both C. fragile and C. cylindricum showed a decreasing trend, and the low light intensity group (10−30 μmol/(m2∙s)) had higher photosynthetic efficiency than the high light intensity group (60−120 μmol/(m2∙s)), with significant differences. The decrease in Fv/Fm indicates that PSII was damaged by light-intensity stress, which reduced the primary light energy transformation efficiency of PSII, damaged the PSII active center, and inhibited the primary reaction of photosynthesis (Hui et al., 2004). This may be because the transfer of photosynthetic electrons from the PSII reaction center to QA and other pools is affected by excessive light intensity, and the PSII active center is damaged (Yang et al., 2004). Similarly, high light intensity also affects the ability of algae to respond to light (Ma et al., 2006), as the rETRmax of thalli is significantly reduced at high light intensities (120 μmol/(m2∙s)).
When plants capture more light energy than they need for photosynthesis, the excess energy is dissipated through NPQ to protect photosynthetic structures from damage (Maxwell and Johnson, 2000). Goss et al. (1998) suggested that NPQ reflects the strength of the radiationless energy dissipation pathway of the xanthophyll cycle. The xanthophyll cycle promotes the conformational change of photosystem II light-harvesting complexes (LHCII) from the “light-funnel” state to the “energy-consuming” state (Ruban et al., 1994). The results of this study showed that high light intensity caused an increase in the NPQ curve of C. fragile, indicating that as the photosynthetic capacity of the thalli decreased, more energy was consumed in the form of thermal energy. The excess light energy absorbed by the thalli can also be consumed through the molecular oxygen uptake pathway, which directly results in a large production of various reactive oxygen species (ROS) (Ciompi et al., 1996). It further causes damage to the cell membrane system and peroxidation of membrane lipids, and even leads to cell death (Van Breusegem et al., 2001). In contrast, the NPQ curve of C. cylindricum decreased at a high light intensity, and thus the excess light energy was likely to be consumed by the molecular oxygen uptake pathway. It is probably because of this that the total antioxidant capacity of the thalli decreased significantly under high light intensity.
In the light range of 10−120 μmol/(m2∙s), the MDA of C. fragile increased with the increase of light intensity. The MDA content was higher at high light intensities (90−120 μmol/(m2∙s)) but was not significantly different from the low light intensity group. In contrast, C. cylindricum showed essentially the opposite trend in the same light intensity range, with its MDA content decreasing with increasing light intensity. This implies that the degree of membrane lipid peroxidation in C. fragile increases with increasing light intensity, while the opposite is essentially true for C. cylindricum. Carotenoids protect plant cells and tissues from photo-oxidative damage by scavenging reactive oxygen species through physical and chemical reactions (Maoka, 2020). The carotenoids of C. fragile showed an increasing trend in the light range of 30−120 μmol/(m2∙s). In contrast, no significant differences were found in the carotenoid content of C. cylindricum in the light range of 10−120 μmol/(m2∙s). Therefore, it can be speculated that C. fragile can resist the oxidative damage to thalli cells by strong light through the accumulation of carotenoids under a high light intensity environment, and mitigate the degree of membrane lipid peroxidation to a certain extent.
Algae have antioxidant systems that resist external damage, including enzymes and small-molecule antioxidant substances (Zubia et al., 2007). POD is the main enzyme that decomposes H2O2 into water (H2O) and is a component of the antioxidant system and a component of the protective enzyme system (Velikova et al., 2000). The level of POD activity affects the decomposition of hydrogen peroxide and other peroxides. Peroxides in plants are toxic substances, and low concentrations of peroxides are also capable of blocking photosynthesis (Du et al., 2001). In the light intensity range of 10−120 μmol/(m2∙s), the POD activity of both C. fragile and C. cylindricum showed an increasing trend with light enhancement. At lower light intensities (10−30 μmol/(m2∙s)), the POD activity of C. fragile was significantly higher than that of C. cylindricum. Moreover, low light intensity (10 μmol/(m2∙s)) and high light intensity (120 μmol/(m2∙s)) had no significant effect on the T-AOC of C. fragile, but the T-AOC of C. cylindricum was significantly reduced. We speculate that the self-protective ability of C. fragile may be stronger than that of C. cylindricum at low and high light intensities and that the high peroxidase activity and stable total antioxidant capacity of C. fragile at high light intensities may mitigate the effects of increased membrane lipid peroxidation.
It can be inferred that in coastal China, C. fragile can improve light energy utilization (α) to increase the Fv/Fm of the thalli in winter when light intensity is reduced. Under the enhanced light intensity in summer, the damage caused by photoinhibition can be reduced or avoided by increasing the Ek and qP in C. fragile. The self-protection ability of C. cylindricum at low and high light intensities may be weaker than that of C. fragile. Under high light intensity, the photosynthetic activity of C. cylindricum decreases, and thus it disappears in mid-July along the southern coast of China. In winter, when light intensity is reduced, C. cylindricum can improve photosynthetic efficiency by increasing light energy utilization (α) and accumulating pigment content. In general, the adaptation to light differs between C. fragile and C. cylindricum. Compared to C. cylindricum, C. fragile is better adapted to different light intensities, especially at high light intensities, where C. fragile is significantly more adaptable than C. cylindricum. The results are to some extent consistent with the tidal distribution characteristics of these two species of Codium, with the C. fragile mostly distributed in the intertidal area with stronger light intensity and the C. cylindricum mostly distributed in the lower intertidal to subtidal area with weaker light intensity. At the same time, the results of this study can also explain why C. fragile can widely invade the world from the perspective of light intensity, while the C. cylindricum did not become a widespread invasive species. However, during the change of seasons, the temperature, salinity, and nitrogen source of the environment will also change, and temperature, light, salinity, and nitrogen source all have different degrees of influence on the growth of Codium (Hanisak, 1979). Therefore, to further understand the environmental adaptations of C. fragile under seasonal changes and the reasons why it can successfully invade worldwide, it is especially important to study the effects of other environmental factors such as temperature, salinity, and nutrient salts on it, which also points the way to our next work.
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Figure 1. Map of the distribution of the sampling stations in Shengsi Archipelago. The image labeled the identification numbers for the sampling stations, where Jun, Aug, Nov, and Apr represent different sampling times (June 2010, August 2010, November 2020, and April 2021, respectively).
Figure 2. Species richness (S) and their assemblage composition in Shengsi Archipelago. a. Macrobenthic assemblage composition in general. b. Temporal variation in macrobenthos diversity and assemblage composition. The 'others' category classification includes nemerteans, echiurans, and fish. Jun, Aug, Nov, and Apr represent different sampling times (June 2010, August 2010, November 2020 and April 2021, respectively).
Figure 3. Temporal changes in the average abundance (a), biomass (b), and their composition in the Shengsi Archipelago. Jun, Aug, Nov, and Apr represent different sampling times (June 2010, August 2010, November 2020, and April 2021, respectively).
Figure 4. Temporal variation in diversity indices of microbenthic community in the Shengsi Archipelago. Jun, Aug, Nov, and Apr represent different sampling times (June 2010, August 2010, November 2020, and April 2021, respectively). d, H' and J represent the Margalef richness index, Shannon-Wiener diversity index, and Pielou evenness index, respectively. Different letters (a, b) indicate significant differences (p < 0.05) in these indices between different months.
Figure 5. CCA Analysis Results for community-environment correlation. The abundance of dominant species in the stations of Jun11, Aug02, Aug05 and Aug11 was 0. Therefore, these stations were omitted from the analysis. The abbreviations in the figure were formed using the first three letters of the genus name and the first two letters of the specific epithet. Polychaete Sternaspis chinensis is abbreviated as STECH, polychaete Aglaophamus dibranchis as AGLDI, mollusk Eocylichna braunsi as EOCBR, mollusk Endopleura lubrica as ENDLU, polychaete Tharyx multifilis as THAMU, polychaete Nephtys oligobranchia as NEPOL, polychaete Sigambra hanaokai as SIGHA, polychaete Prionospio sp. as PRISP, polychaete Mediomastus sp. as MEDSP, crustacean Eriopisella sechellensis as ERISE, echinoderm Amphiura vadicola as AMPVA, polychaete Heteromastus filiformis as HETFI, and polychaete Lumbrineris japonica as LUMJA.
Table 1. Temporal variations of environmental variables in the waters of Shengsi Archipelago
Environmental Variables June August November April Hg/mg·kg–1 0.020 (0.001) a 0.020 (0.001) a 0.077 (0.014) b No data Pb/mg·kg–1 25.4 (0.6) a 24.7 (0.6) a 19.9 (0.4) b No data As/mg·kg–1 5.5 (0.1) a 5.6 (0.2) a 9.5 (0.6) b No data D/um 9.8 (0.4) a 12.7 (0.8) b 11.6 (0.7) ab No data Depth/m 13.2 (1.8) a 17.5 (6.0) a 13.3 (1.9) a 13.7 (2.7) a Temperature/℃ 19.4 (0.1) a 25.1 (0.3) b 20.2 (0.1) c 16.3 (0.2) d Salinity/‰ 20.6 (0.8) a 21.9 (0.7) a 27.2 (0.7) b 28.3 (0.7) b SPM/mg·L–1 40 (15) a 18 (2) a 235 (43) b 604 (90) c Chl a/μg·L–1 3.23 (0.77) a 15.61 (4.01) b No data No data The standard error for each value is indicated in brackets. Superscripts (a, b, c, d) are used to indicate whether there is a significant difference in the environmental variables among different months. Superscripts with the same letter indicate non-significant differences (p > 0.05), whereas different letters indicate significant differences (p < 0.05). 
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Table 2. Temporal variation in the average abundance of dominant species in Shengsi Archipelago
Dominant Species June August November April Aglaophamus dibranchis/ind.·m–² 6.7 (3.1)* 8.2 (4.2)* 0 0 Sternaspis chinensis/ind.·m–² 23.8 (7.9)* 14.5 (5.8)* 8.0 (2.7)* 9.1 (3.4)* Eocylichna braunsi/ind.·m–² 5.8 (2.2)* 6.4 (3.2) 0.5 (0.5) 0.5 (0.5) Endopleura lubrica/ind.·m–² 2.9 (1.1) 79.1 (54.2)* 0 0 Tharyx multifilis/ind.·m–² 0 0 11 (3.4)* 0 Nephtys oligobranchia/ind.·m–² 0 0 10.5 (3.7)* 5.9 (2.5)* Sigambra hanaokai/ind.·m–² 0 0 29.5 (7.3)* 0.9 (0.6) Prionospio sp. /ind.·m–² 0 0 14.0 (4.8)* 0 Mediomastus sp./ind.·m–² 0 0 12.0 (5.6)* 0 Eriopisella sechellensis/ind.·m–² 0 0 10.0 (5.8)* 0 Amphiura vadicola/ind.·m–² 4.5 (1.8) 4.1 (2.4) 19.0 (15.8)* 8.6 (3.1)* Lumbrineris japonica/ind.·m–² 0 0 0 4.5 (1.6)* Dentinephtys glabra/ind.·m–² 0 0 0 9.5 (4.4)* Heteromastus filiformis/ind.·m–² 0.8 (0.8) 0 0 11.8 (5.7)* The standard error for each value is indicated in brackets. The dominant species in the corresponding month are marked with *.
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Table 3. Average dissimilarity and ANOSIM analysis results of macrobenthic communities in the Shengsi Archipelago between different months
Groups Average dissimilarity (%) R p value Jun&Aug 83.37 −0.003 0.468 Jun&Nov 93.68 0.658 0.001*** Jun&Apr 90.54 0.401 0.001*** Aug&Nov 95.29 0.660 0.001*** Aug&Apr 93.03 0.456 0.001*** Nov&Apr 88.48 0.662 0.001*** Jun, Aug, Nov, and Apr represent different sampling times (June 2010, August 2010, November 2020, and April 2021, respectively). *p < 0.05 (significantly different); **p < 0.01 (very significant); ***p < 0.001 (extremely significant).
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Table 4. SIMPER analysis results: key differentiating species and their contribution rates
Key differentiating species Jun&Aug Jun&Nov Jun&Apr Aug&Nov Aug&Apr Nov&Apr Endopleura lubrica/% 9.7 1.91 2.48 7.31 9.07 0 Sternaspis chinensis/% 7.68 5.75 7.5 4.56 5.91 4.03 Amphiura vadicola/% 4.39 4.31 5.17 4.21 5.07 5.56 Heteromastus filiformis/% 0.4 0.32 5.44 0 5.03 4.44 Sigambra hanaokai/% 0 9.05 0.77 8.55 0.72 9.06 Prionospio sp./% 0 4.93 0 4.68 0 5.3 Tharyx multifilis/% 0 4.79 0 4.52 0 5.14 Only species with contributions ≥ 4% in any given month are listed. Jun, Aug, Nov, and Apr represent different sampling times (June 2010, August 2010, November 2020, and April 2021, respectively).
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