Impact of light and temperature on the uptake of algal symbionts by coral juveniles

Abstract

The effects of temperature and light on the breakdown of the coral-Symbiodinium symbiosis are well documented but current understanding of their roles during initial uptake and establishment of symbiosis is limited. In this study, we investigate how temperature and light affect the uptake of the algal symbionts, ITS1 types C1 and D, by juveniles of the broadcast-spawning corals Acropora tenuis and A. millepora. Elevated temperatures had a strong negative effect on Symbiodinium uptake in both coral species, with corals at 31 °C showing as little as 8% uptake compared to 87% at 28 °C. Juveniles in high light treatments (390 µmol photons m(-2) s(-1)) had lower cell counts across all temperatures, emphasizing the importance of the light environment during the initial uptake phase. The proportions of the two Symbiodinium types taken up, as quantified by a real time PCR assay using clade C- and D-specific primers, were also influenced by temperature, although variation in uptake dynamics between the two coral species indicates a host effect. At 28 °C, A. tenuis juveniles were dominated by C1 Symbiodinium, and while the number of D Symbiodinium cells increased at 31 °C, they never exceeded the number of C1 cells. In contrast, juveniles of A. millepora had approximately equal numbers of C1 and D cells at 28 °C, but were dominated by D at 30 °C and 31 °C. This study highlights the significant role that environmental factors play in the establishment of coral-Symbiodinium symbiosis and provides insights into how potentially competing Symbiodinium types take up residence in coral juveniles.

Figure 1. Visual assessment of Symbiodinium uptake.

Juveniles were scored in two categories (white or pigmented) according to pigmentation levels. The specimen on the left is a typical “white” juvenile while the two on the right represent a range of “pigmented” juveniles.

Figure 2. Pigmentation ratios (±1 SE) of coral juveniles kept at 28, 30, or 31°C and under high light (a,b; 390 µmol photons m⁻² s⁻¹) or low light (c,d; 180 µmol photons m⁻² s⁻¹) levels.

Pigmentation ratios were calculated after 10 (A. tenuis a, c) or 15 (A. millepora b, d) days of exposure to Symbiodinium, and again after a further 10 or 15 days in filtered sea water (1 µm) without additional exposure to Symbiodinium. See Table 1 for sample sizes.

Figure 3. Symbiodinium cell counts in A. tenuis juveniles kept at 28, 30, or 31°C and under high light (a, 390 µmol photons m⁻² s⁻¹) or low light (b, 180 µmol photons m⁻² s⁻¹) levels.

The number of cells was calculated from 10 replicate counts for each of 12 samples per treatment per day. Cell counts (±1 SE) were normalized to the number of polyps taken by each sample.

Figure 4. Relative survival (±1 SE) of juveniles in the 28, 30, or 31°C treatments and under high light (390 µmol photons m⁻² s⁻¹) or low light (180 µmol photons m⁻² s⁻¹) levels for: (a) Acropora tenuis after 20 days, and (b) A. millepora after 30 days.

See Table 1 for sample sizes.

Figure 5. Change in Symbiodinium D∶C cell ratios (±1 SE) over time in Acropora tenuis juveniles at 28, 30, or 31°C in: (a) high light (390 µmol photons m⁻² s⁻¹), or (b) low light levels (180 µmol photons m⁻² s⁻¹).

Dotted line represents equal proportions of Symbiodinium types D and C cells within the juveniles. Ratios closer to 1 are dominated by type D; ratios closer to 0 are dominated by type C. N = 20 per data point.

Figure 6. Change in Symbiodinium D∶C cell ratios (±1 SE) over time in Acropora millepora juveniles at 28, 30, or 31°C in: (a) high light (390 µmol photons m⁻² s⁻¹), or (b) low light levels (180 µmol photons m⁻² s⁻¹).

Dotted line represents equal proportions of Symbiodinium types D and C cells within the juveniles. Ratios closer to 1 are dominated by type D; ratios closer to 0 are dominated by type C. N = 10 per data point.

Figure 7. Long term sea temperature at 2 m depth in Geoffrey Bay, Magnetic Island.

Data was collected over 15 years (1996–2011) by loggers maintained by the Australian Institute of Marine Science (Channel ID 1820, data available from http://data.aims.gov.au/gbroosdata/services/rss/channel/923/150).