Physiological functional traits explain morphological variation of Ulva prolifera during the drifting of green tides

Abstract

Ulva prolifera green tides, one of the greatest marine ecological disasters, originate in the southern Yellow Sea of China and obtain the highest biomass in Haizhou Bay (latitude around 35° N) during northward drift. U. prolifera shows different morphologies from southern Haizhou Bay (SH) to northern Haizhou Bay (NH). Owing to the distinct nutrient environments between SH and NH, we hypothesized that thalli in NH with poor nutrients increased the surface area to volume ratio (SA:VOL) to better absorb nutrients. Here, we tested this hypothesis by comparing the SA:VOL of thalli in SH and NH. The results showed that the thalli in NH had a lower SA:VOL than those in SH, and SA:VOL had positive relationships with temperature and nutrients, contrary to the general hypothesis. The novel results suggested that morphological differences of U. prolifera were the result of developmental state rather than environmental acclimation. Indicators of reproduction (reproductive allocation ratio) were negatively related to variation in tissue contents of C, N, P, and crude protein, whereas indicators of growth (tissue contents of C, N, P, and crude protein) showed significant positive influences on SA:VOL. The results indicated that a trade-off relationship between reproduction and growth existed in the northward drift. All the results suggested that physiological functional traits affected morphological variation of U. prolifera in different environmental conditions during the drifting of green tides. This study presents new insights into the opportunist species nature of U. prolifera through morphological variation and associated functional consequences.

Keywords: Ulva prolifera; morphological variation; photosynthetic system; reproductive allocation; surface area to volume ratio.

FIGURE 1

Locations of sampling sites in the southern area (SH; A/B/C) and northern area (NH; D/E/F) of Haizhou Bay (latitude around 35°N), Yellow Sea, China

FIGURE 2

Morphology of Ulva prolifera thalli from the southern area (SH) and northern area (NH) of Haizhou Bay, Yellow Sea. (a) Morphology of thalli sampled from the SH. (b) Morphology of thalli sampled from the NH. (c) and (e) The surface areas of thalli in SH were calculated by ImageJ. (d) and (f) The surface areas of thalli in NH were calculated by ImageJ. Bars = 50 mm

FIGURE 3

Morphological variation of Ulva prolifera thalli from the southern area (SH) and northern area (NH) of Haizhou Bay, Yellow Sea. Cellular details of thalli from the SH (bars: a, 50 µm; c, 20 µm) and the NH (bars: b, 50 µm; d, 20 µm)

FIGURE 4

The values of SA:VOL of Ulva prolifera thalli from the southern area (SH; a–c) and northern area (NH; d–f) of Haizhou Bay, Yellow Sea. (a) SA:VOL of thalli. Values are means ± SD (n = 9). Different letters above bars indicate a significant difference (one‐way ANOVA, p < .05). (b) Relationship of mean (±SD) surface area to volume ratio (SA:VOL) of Ulva prolifera thalli from the sampling lines (a–f). Solid lines are the regression fits from the six sampling lines (p < .05; n = 9)

FIGURE 5

The values of RGR of Ulva prolifera thalli from the southern area (SH; a–c) and northern area (NH; d–f) of Haizhou Bay, Yellow Sea. Values are means ± SD (n = 9). Different letters above bars indicate a significant difference (one‐way ANOVA, p < .05)

FIGURE 6

Photosynthetic parameters of Ulva prolifera thalli from the southern area (SH) and northern area (NH) of Haizhou Bay, Yellow Sea. (a) Box‐plot of F_v /F_m and Y(II). Values are means ± SD (n = 27). *Significant correlation at the 0.05 level. (b) Rapid light–response curves of the mean relative electron transport rate (rETR) versus photosynthetically active radiation (PAR) of Ulva prolifera thalli from the southern area (SH) and northern area (NH) of Haizhou Bay, Yellow Sea. Values are means ± SD (n = 27)

FIGURE 7

Biochemical parameters of Ulva prolifera thalli from the southern area (SH) and northern area (NH) of Haizhou Bay, Yellow Sea. (a) Box‐plots of tissue elemental analysis (C, N, and P). Values are means ± SD (n = 27). *Significant correlation at the 0.05 level. (b) Box‐plots of crude protein, crude fiber, and crude lipid. Values are means ± SD (n = 27). *Significant correlation at the .05 level

FIGURE 8

Box‐plots of reproductive allocation ratio (RA) of Ulva prolifera thalli collected from the southern area (SH) and northern area (NH) of Haizhou Bay, Yellow Sea. Values are means ± SD (n = 27). Different letters above boxes indicate a significant difference (Student's t‐test, p < .05)

FIGURE 9

Redundancy analysis based on different environmental and physiological parameters of Ulva prolifera (n = 3 individuals per site) at the six study lines. Red arrows show environmental factors, and blue arrows show physiological functions of U. prolifera

FIGURE 10

Correlation analysis between environmental factors and physiological parameters of Ulva prolifera. Different colors indicate different levels of the Pearson correlation coefficient. *Significant correlation at the .05 level. **Significant correlation at the .01 level

FIGURE 11

Relationships between mean (±SD) photosynthesis parameters (a), tissue of C (b), N (c), P (d) content, crude fiber (e), crude protein (f), crude lipid (g), RGR (h), and RA (i), and SA:VOL at each of the six study lines. Solid lines are the regression fits to data from study sites (p < .05, n = 9)

FIGURE 12

Pathway analysis using PLS‐SEM on influential factors of SA:VOL. Solid lines mean a significant influence. *Significant correlation at the .05 level. **Significant correlation at the .01 level