Received 10 November 2015, accepted 18 December 2015, DOI: 10.1111/php.12567. ABSTRACT. Ultraviolet radiation (UVR, 280â400 nm) is one of the poten-.
Photochemistry and Photobiology, 2016, 92: 293–300
Incident Ultraviolet Irradiances Influence Physiology, Development and Settlement of Larva in the Coral Pocillopora damicornis Jie Zhou1, Tung-Yung Fan2,3, John Beardall1,4 and Kunshan Gao*1 1
State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, Fujian, China National Museum of Marine Biology and Aquarium, Pingtung, Taiwan 3 Institute of Marine Biology, National Dong Hwa University, Pingtung, Taiwan 4 School of Biological Sciences, Monash University, Clayton, Vic., Australia 2
Received 10 November 2015, accepted 18 December 2015, DOI: 10.1111/php.12567
ABSTRACT
Pocillopora damicornis and Symbiodinium could extend the vitality of larvae. Later Isomura and co-workers (5) showed that planulae of brooding coral species could live longer in the light than when left in the dark. In spite of the importance of light for coral larvae, studies related to the function of photosynthesis in symbiotic algae during the period of presettlement are rare. Whether the symbiotic algae provide energy to the larval host by photosynthesis or just as food, the evidence showed that the presence of zooxanthellae could indeed enhance the survivorship of planula larvae. This is a significant issue, as sufficient larval recruitment is critical to sustaining reefs and the dispersal of corals into refugia, especially when their original environment is less habitable due to local stressors and global change. However, the environmental conditions around planula larvae are quite distinct from that of their parental corals. As with other zooplankton, although they can swim, coral planula larvae often float with the movement of seawater, and therefore will encounter variable disturbances such as increased temperatures, predation by other creatures and exposure to high-intensity solar radiation. Tropical scleractinian corals, with associated algae, are usually distributed in clear, shallow water, typically at depths shallower than 60 m where the water attenuation of photosynthetically active radiation (KPAR) is usually lower than 0.2 m1, which exposes them to high levels of solar radiation (6,7). Although the attenuation coefficient for downwelling irradiance and penetration depth [which depends on the optical properties of the water, dissolved material, phytoplankton concentration and local meteorological or cloud cover (8)] vary from area to area, ultraviolet radiation (UVR, 280–400 nm) is usually attenuated at least two times faster than PAR. However, the oligotrophic properties of coral reef waters means that 1% of incident surface UVA (315–400 nm) and UV-B (280–315 nm) irradiances could penetrate as deep as 12 m and 8.4 m (Yongxing Island, South China Sea, China) (9), or 22 m and 12 m (Heron Reef, southern Great Barrier Reef, Australia) (7) respectively. Thus, for shallow tropical corals, especially those found at 0.05). Thus, UV radiation clearly inhibited the development of coral larvae. Pigment content and Symbiodinium density Four cohorts of coral were used for pigment content analysis. However, among the four cohorts, only the group released in
Figure 1. Effects of 4 days exposure of Pocillopora damicornis larvae to UVR treatments on the percentage that either survived (a), metamorphosed (b) or settled (c). Data are means SD (n = 3 for all treatments with 25 larvae each); treatment means marked with asterisks differ significantly (Fisher’s LSD post hoc analysis, P < 0.05).
August showed an obvious decrease in chl a content per larva in the PAB treatment compared to the P treatment (F2,6 = 5.605, P = 0.04, Fig. 2a). UV exposure did not result in any significant variation in pigment content per symbiont cell, or in concentration of carotenoids or UVAC in larvae (data not shown). To explore the differences in the UV effect among cohorts, correlations were conducted between P values, i.e. the significance of difference among the pigment contents, and temperature or irradiance. As a result, a positive relationship was uncovered between the significance of UV-induced reduction in chl a per larva and temperature (Fig. 2b). Specifically, as the temperature increased, the P value of one-way ANOVA decreased (R2 = 0.86, Pearson’s r = 0.95, P = 0.05), i.e. the difference among treatments was more distinguishable. A stronger relationship was found when the comparison was only made for differences between P and PAB treatments, in which the R2 was as high as 0.99, with P = 0.003 (Fig. 2b inset graph). Furthermore, irradiance level also affected the significance of the UV effect on chl a concentration. The UV-A-induced chl a decrease appeared significant only at doses over 0.76 MJ m2 according to the linear regression equation (R2 = 0.95, Pearson’s r = 0.98, P = 0.02, Fig. 2c). UV-absorbing compounds were detected in all treatments, and their content in larvae was relatively high, even without exposure to UV radiation. Although there was no evident change in UVAC content detected among the four cohorts, its content in coral larvae did show positive correlation with temperature when UV radiation was filtered (R2 = 0.85, Pearson’s r = 0.95,
Photochemistry and Photobiology, 2016, 92
Figure 2. Chl a concentration of the August cohort (a), the relationship between temperature and P values from ANOVA statistical analysis of the effects of UV radiation on larval chl a content (b) and the correlation between UV-A dose and P values from Fisher’s LSD analysis with the comparison between P and PA treatments (c). The inset graph in (b) shows the P value from Fisher’s LSD between P and PAB treatment, and the different letters indicate significant differences among the irradiance treatments at P < 0.05. Values of chl a are means SD (n = 3 for all treatments with 20 larvae each).
P = 0.05, Fig. 3a). In the P treatment, the UVAC concentration in larvae was over 1.5 times higher than that of chl a, and with the increase in temperature the ratio became higher (R2 = 0.94, Pearson’s r = 0.98, P = 0.02, Fig. 3b). Similar to chl a, the P value from one-way ANOVA also had a negative relationship with temperature (R2 = 0.86, Pearson’s r = 0.95, P = 0.05, Fig. 3c), indicating that high temperature induced notable differences in UVAC synthesis among treatments. After short-term UVR exposure, the mean Symbiodinium density remaining in the larvae varied from 0.76 0.04 9 104 to 2.36 0.19 9 104 cells per larva, but no significant difference was detected among the three treatments. At the same time, there was no evident variation observed in chl a concentration in the rearing seawater, with mean concentrations of 2.80 0.09, 2.54 0.46 and 2.61 0.45 ng mL1 for P, PA and PAB treatments respectively (F2,6 = 0.385, P = 0.70). Photosynthetic rate and respiration The photosynthetic rate and photosynthetic efficiency were determined to evaluate the photophysiology of symbiotic algae in larvae under UVR stress. The results of oxygen evolution revealed that Pnet was significantly reduced when larvae were exposed to UV-A plus UV-B, compared to those only exposed
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Figure 3. UVAC content and the ratio of UVAC: Chl a in coral larvae exposed only to PAR as a function of temperature (a, b), and the relationship between temperature and P values from ANOVA statistical analysis of the effects of UV radiation on larval UVAC content (c). Values of UVAC content are means SD (n = 3 for all treatments with 20 larvae each).
to UV-A (F2,6 = 11.068, P = 0.01, Fig. 4a; F2,6 = 5.201, P = 0.05, Fig. 4b). While the Pgross per larva showed a similar pattern (F2,6 = 5.091, P = 0.05, Fig. 4b), the same parameter normalized to algal density displayed an increase when exposed to UV-A (F2,6 = 22.866, P = 0.001, Fig. 4a), reflecting the variations in algal density among the samples within the treatment. Using the LEDR values for respiration, the Pgross 0 per cell presented the same trend as Pgross (F2,6 = 11.766, P = 0.01, Fig. 4a), while the difference in Pgross 0 per larva between the P and PAB treatments was greater, and both the P and PA treatments showed significantly higher rates than the PAB treatment (F2,6 = 13.191, P = 0.01, Fig. 4b). However, there was no change in the photosynthetic efficiency of PSII between treatments, and the mean values of Fv’/Fm’ were 0.48 0.06, 0.44 0.06 and 0.51 0.13 for P, PA and PAB treatments, respectively (F2,6 = 0.456, P = 0.65), with those of Fv/Fm being 0.52 0.09, 0.53 0.07 and 0.53 0.07 for the three treatments (F2,6 = 0.012, P = 0.99). In the analyses of respiration, though the dark respiration rate appeared to show a similar trend to Pnet, i.e. the rate decreased in the PAB treatment, the change was not statistically significant (F2,6 = 1.300, P = 0.34, Fig. 4c). Similarly, no variation in LEDR was observed between treatments (F2,6 = 1.160, P = 0.37) and the P/R ratios were not distinctive among treatments (F2,6 = 1.470, P = 0.30), although the mean value seemed to be lower in the PAB (P/R = 0.4 0.6) compared to P (P/R = 1.7 1.4) and PA treatments (P/R = 1.2 0.6).
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Figure 4. Photosynthetic oxygen evolution rate (a, b) and respiration rate (c) of larva after exposure to PAR (P, white), PAR + UV-A (PA, gray) and PAR + UV-A + UV-B (PAB, black) treatments for 6 h. (a) pmol O2 cell1 min1; (b) nmol O2 larva1 min1; (c) dark respiration and light-enhanced dark respiration (LEDR). The different letters indicate significant differences among treatments at P < 0.05. Values are means SD (n = 3 for all treatments with ~25 larvae each).
DISCUSSION In the present work, the presence of UV-B in addition to UV-A brought about a 75–85% reduction in the net photosynthesis of the symbiotic algae, and no effect of either UV-A or UV-B on respiration was observed (Fig. 4). Although the pigment content and Symbiodinium density were not affected by the UV exposure when the temperature was lower than 30°C, the presence of UVA significantly decreased the larval survivorship, though addition of UV-B did not lead to further decline of the survivorship; similar effects were found in metamorphosis or settlement after the 4 day exposures (Fig. 1). In fact, the correlation analysis showed that both the concentrations of chl a and UVAC had a relationship with temperature. The larval development was severely inhibited by UV radiation (Fig. 1). This result is consistent with previous studies on both brooding and broadcast-spawning coral species (18–20). However, since none of the differences in survivorship, metamorphosis or settlement between PA and PAB treatment were significant, the influence of UV-B could be negligible here. In Acropora palmate, a similar pattern was observed in that the survivorship of larvae released from shallow waters (
