Mesophotic corals in Hawai'i maintain autotrophy to survive low-light conditions

Abstract

In mesophotic coral ecosystems, reef-building corals and their photosynthetic symbionts can survive with less than 1% of surface irradiance. How depth-specialist corals rely upon autotrophically and heterotrophically derived energy sources across the mesophotic zone remains unclear. We analysed the stable carbon (δ¹³C) and nitrogen (δ¹⁵N) isotope values of a Leptoseris community from the 'Au'au Channel, Maui, Hawai'i (65-125 m) including four coral host species living symbiotically with three algal haplotypes. We characterized the isotope values of hosts and symbionts across species and depth to compare trophic strategies. Symbiont δ¹³C was consistently 0.5‰ higher than host δ¹³C at all depths. Mean colony host and symbiont δ¹⁵N differed by up to 3.7‰ at shallow depths and converged at deeper depths. These results suggest that both heterotrophy and autotrophy remained integral to colony survival across depth. The increasing similarity between host and symbiont δ¹⁵N at deeper depths suggests that nitrogen is more efficiently shared between mesophotic coral hosts and their algal symbionts to sustain autotrophy. Isotopic trends across depth did not generally vary by host species or algal haplotype, suggesting that photosynthesis remains essential to Leptoseris survival and growth despite low light availability in the mesophotic zone.

Keywords: Leptoseris; mesophotic coral ecosystems; niche partitioning; photoacclimatization; stable isotopes; trophic strategy.

Figure 1.

Heterotrophy plays a dominant role in Leptoseris nutrition, but host and symbiont stable isotope values converge across mesophotic depths. (a) SIBER model outputs for δ¹³C, δ¹⁵N values of all samples with dotted lines denoting convex hulls of hosts (orange) and symbionts (teal). Solid rings of the same colours denote standard ellipse areas corrected for sample size (SEA_C). (b) Isotopic values for hosts and symbionts pooled by 5 m collection depth bins (means ± s.e.; electronic supplementary material, table S4).

Figure 2.

Carbon exchange between hosts and symbionts remains constant for most Leptoseris genotypes across depth, supporting sustained reliance on autotrophy. δ¹³C (‰) of (a) host, (b) symbionts and (c) differences between host and symbiont isotopic values for the Leptoseris community across depth (m). Points indicate means ± s.e., binned by collection depth and jittered for clarity. Solid lines show significant linear regressions (p < 0.05; electronic supplementary material, table S2). Dashed lines in a and b represent the overlayed regressions for symbionts and hosts, respectively. The red shaded area indicates the difference between host and symbiont δ¹³C values plotted in c. Trend lines in a and b show host δ¹³C was consistently about 0.5‰ lower than symbiont δ¹³C across depths. The same data by (d–f) host species or (g–i) symbiont haplotype show host and symbiont δ¹³C and the difference between them. Re-categorizing points changed some of their values and total counts across plots. Dashed lines in d–e and g–h indicate the community trends shown in a and b, respectively. Solid lines show significant linear regressions for host species (d–f) and algal haplotype (g–i) (p < 0.05; electronic supplementary material, table S2). Zero-lines (grey) in c, f and i indicate no isotopic difference between host and symbiont fractions.

Figure 3.

Host δ¹⁵N and symbiont δ¹⁵N converge across depth, providing further evidence for sustained autotrophic reliance through the mesophotic zone. δ¹⁵N (‰) of (a) host, (b) symbionts and (c) differences between host and symbiont isotopic values for the Leptoseris community across depth (m). Points indicate means ± s.e., binned by collection depth and jittered for clarity. Solid lines show significant linear regressions (p < 0.05; electronic supplementary material, table S2). Dashed lines in a and b represent the overlayed regressions for symbionts and hosts, respectively. The red shaded area indicates the difference between host and symbiont δ¹⁵N values plotted in c. Trend lines in a and b show that host δ¹⁵N decreased and symbiont δ¹⁵N increased across depths, converging at approximately 4‰ at 125 m. The same data by (d–f) host species or (g–i) symbiont haplotype show host and symbiont δ¹⁵N and the difference between them. Re-categorizing points changed some of their values and total counts across plots. Dashed lines in d,e and g,h indicate the community trends shown in a and b, respectively. Solid lines show significant linear regressions for host species (d–f) and algal haplotype (g–i) (p < 0.05; electronic supplementary material, table S2). Zero-lines (grey) in c, f, and i indicate no isotopic difference between host and symbiont fractions.

Figure 4.

Together, δ¹³C and δ¹⁵N explain how nitrogen exchange supports autotrophy at depth. Schematic hypothesis for our results across collection depth. Leptoseris hosts can obtain carbon and nitrogen heterotrophically, most likely from POM. Symbionts can supply carbon and nitrogen to hosts autotrophically by taking dissolved inorganic carbon and nitrogen from the water column and translocating photosynthates (PS) to the host. (a) At 65 m, with abundant nitrogen (N), ${\mathrm{NH}}_4^{+}$ waste can be excreted from the coral and/or symbionts. Symbionts do not readily share/exchange N with the host due to high abundance of N. Preferential excretion of ${\hspace{0.17em}}^{14}{\mathrm{NH}}_4^{+}$ and limited N sharing increase host δ¹⁵N; as ¹⁴N is excreted, host ¹⁵N : ¹⁴N increases. Symbiont δ¹⁵N remains low as symbionts transfer less N to hosts, producing lower symbiont ¹⁵N : ¹⁴N. Heterotrophy contributes more to Leptoseris energy inputs than autotrophy (figure 1). However, relative carbon exchange between hosts and symbionts is consistent across depth (i.e. symbiont δ¹³C approximately 0.5‰ higher than host δ¹³C across depth; figure 2). Therefore, high heterotrophy on POM that supplies high nitrogen inputs at 65 m corresponds with proportionally high rates of autotrophy. (b) At 100 m, weak currents limit POM, so Leptoseris increase N exchange between host and symbionts. Excretion is limited and hosts share higher amounts of ${\hspace{0.17em}}^{14}{\mathrm{NH}}_4^{+}$ waste to the symbionts (larger ${\hspace{0.17em}}^{14}{\mathrm{NH}}_4^{+}$ arrow towards Sym). Symbionts transfer more N to hosts. N exchange homogenizes host and symbiont ¹⁵N : ¹⁴N ratios, decreasing host δ¹⁵N and increasing symbiont δ¹⁵N compared with 65 m (figures 3 and 4a). Since symbiont δ¹³C remains approximately 0.5‰ higher than host δ¹³C (figure 2), reduced heterotrophy at 100 m coincides with a proportional reduction in autotrophy, consistent with light limitation at depth. Leptoseris reefs from the ‘Au‘au Channel, Hawai‘i at (c) 86 m and (d) 100 m (submersible photographs courtesy of the Hawai‘i Undersea Research Laboratory).