Comparative studies on the ecophysiological differences of two green tide macroalgae under controlled laboratory conditions

Abstract

Yellow Sea green tides have occurred in coastal China almost every year from 2007 to 2011. Ulva prolifera (Müller) J. Agardh has been identified as the causative macroalgal species. U. intestinalis, however, has been observed in the bloom areas, co-occurring with U. prolifera, but it has not been found to be causative. The Yellow Sea green tide has shown consistent phases of development that match corresponding environmental changes. U. prolifera, not U. intestinalis, is dominant. Our experimental design was based on these observed phenomena, and the results of our field investigation indicated a close relationship between changes in principal environmental factors (irradiance, temperature, and salinity) and the development of each phase of the bloom. These main environmental factors were simulated to allow estimation and comparison of the physiological responses of U. prolifera and U. intestinalis. Ecophysiological differences were found between these two species. (1) More photosynthetic activity and plasticity were detected in U. prolifera. (2) U. prolifera was found to be more sensitive to dynamic environments, especially harsh and changing environmental conditions. U. intestinalis was found to be more stable, probably due to the higher stress tolerance given by its antioxidant system. (3) Markedly higher nutrient absorption activity was observed in U. prolifera. Comparisons of the ecophysiological traits of these two species in this present study may foster understanding of their natural ecological processes. Specifically, U. prolifera seemed to be more engaged with the ephemeral blooms, while U. intestinalis seemed to be directed toward persistence. This also suggests that the ecological success of U. prolifera may be inextricably linked to its higher capacity for photosynthesis, nutrient absorption, and nutrient assimilation.

Figure 1. In-site investigation of (a) surface seawater salinity (SSS, PSU), mean total rainfall (mm), number of typhoons, and dissolved inorganic nitrogen (DIN, μmol /L); (b) surface seawater temperature (SST, °C), surface seawater salinity (SSS, PSU), and photosynthetically active radiation (PAR, μmol photons.m⁻².s⁻¹).

Total rainfall and number of typhoons were recorded from January 2010 to December 2010. Dissolved inorganic nitrogen (μmol/L) was recorded five times a month from April 2010 to July 2010. Temperature and salinity were measured every week from November 2009 to March 2011. PAR was recorded three times a month from March 2010 to March 2011. Calculated monthly means±standard deviations (SD) are shown. Three different groups of months related to the developmental phases of green tide (pre-bloom, bloom, and post-bloom) are shown as bars. Different color bars and letters indicate significantly different values (P<0.05) as determined by post-hoc multiple comparison testing.

Figure 2.. Relationship between green tide phases (pre-bloom, bloom, and post-bloom) and environmental factors (SST-surface seawater temperature-°C, SSS-surface seawater salinity-PSU and PAR-photosynthetically active radiation-μmol photons.m⁻².s⁻¹) from November 2009 to March 2011 offshore of Qingdao.

Figure 3.. Mean optimal photochemical efficiency of photosynthesis (Fv/Fm) of U. prolifera and U. intestinalis, obtained from short-term (24 h) culture to each, measured under different culture treatments: pre-bloom, bloom, and post-bloom.

Values are means ± SD (n = 5). Different letters above the bars indicate significantly different values (post-hoc, P<0.05)

Figure 4.. Mean optimal photochemical efficiency of photosynthesis (Fv/Fm) of U. prolifera and U. intestinalis, obtained from long-term (7 d) culture to each, measured under different culture treatments: pre-bloom, bloom, and post-bloom.

Values are means ± SD (n = 5). Different letters above the bars indicate significantly different values (post-hoc, P<0.05).

Figure 5. Mean effective quantum yield (Y (II)) of rapid light response curves (RLCs) of U. prolifera and U. intestinalis, obtained from short-term (24 h) culture to each, measured under different culture treatments: pre-bloom, bloom,and post-bloom.

Values are means ± SD (n = 5). Different letters above bars indicate significantly different values (post-hoc, P<0.05).

Figure 6. Mean effective quantum yield (Y (II)) of rapid light response curves (RLCs) of U. prolifera and U. intestinalis, obtained from long-term (7 d) culture, measured under different culture treatments: pre-bloom, bloom, and post-bloom.

Values are means ± SD (n = 5). Different letters above bars indicate significantly different values (post-hoc, P<0.05).

Figure 7. Mean relative electron transport rate (rETR) of rapid light response curves (RLCs) of U. prolifera and U. intestinalis, obtained from short-term (24 h) culture to each, measured under different culture treatments: pre-bloom, bloom, and post-bloom.

Values are means ± SD (n = 5). Different letters above bars indicate significantly different values (post-hoc, P<0.05).

Figure 8. Mean relative electron transport rate (rETR) of rapid light response curves (RLCs) of U. prolifera and U. intestinalis, obtained from long-term (7d) culture, measured under different culture treatments: pre-bloom, bloom, and post-bloom.

Values are mean ± SD (n = 5). Different letters above bars indicate significantly different values (post-hoc, P<0.05).

Figure 9. Mean lipid peroxidation studied as malondialdehyde (MDA) of U. prolifera and U. intestinalis, measured under different culture treatments: pre-bloom, bloom, and post-bloom.

Values are means ± SD (n = 5). Different letters above bars indicate significantly different values (post-hoc, P<0.05).

Figure 10. Mean total soluble protein (TSP) of U. prolifera and U. intestinalis, measured under different culture treatments: pre-bloom, bloom, and post-bloom.

Values are means ± SD (n = 5). Different letters above bars indicate significantly different values (post-hoc, P<0.05).

Figure 11. Mean total antioxidant ability (T-AOC) of U. prolifera and U. intestinalis, measured under different culture treatments: pre-bloom, bloom, and post-bloom.

Values are means ± SD (n = 5). Different letters above bars indicate significantly different values (post-hoc, P<0.05).

Figure 12. Mean activities of antioxidant enzymes superoxide dismutase (SOD) of U. prolifera and U. intestinalis, measured under different culture treatments: pre-bloom, bloom and post-bloom.

Values are means ± SD (n = 5). Different letters indicate significantly different values (post-hoc, P<0.05).

Figure 13. Mean activities of antioxidant enzymes glutathione peroxidase (Gpx) of U. prolifera and U. intestinalis, measured under different culture treatments: pre-bloom, bloom, and post-bloom.

Values are means ± SD (n = 5). Different letters above bars indicate significantly different values (post-hoc, P<0.05).

Figure 14.. Mean activities of non-enzyme antioxidant glutathione (GSH) of U. prolifera and U. intestinalis, measured under different culture treatments: pre-bloom, bloom, and post-bloom.

Values are means ± SD (n = 5). Different letters above bars indicate significantly different values (post-hoc, P<0.05).

Figure 15. Mean activities of N-absorption related enzymes nitrate reductase (NR) of U. prolifera and U. intestinalis, measured under different culture treatments: pre-bloom, bloom, and post-bloom.

Values are means ± SD (n = 5). Different letters above bars indicate significantly different values (post-hoc, P<0.05).