Organic Carbon and Nitrogen Isoscapes of Reef Corals and Algal Symbionts: Relative Influences of Environmental Gradients and Heterotrophy

Abstract

The elemental (C/N) and stable isotopic (δ13C, δ15N) compositions and compound-specific δ15N values of amino acids (δ15NAA) were evaluated for coral holobionts as diagnostic tools to detect spatiotemporal environmental heterogeneity and its effects on coral health. Hermatypic coral samples of eight species were collected at 12 reef sites with differing levels of pollution stress. The C/N ratios, δ13C values, and δ15N values of coral tissues and endosymbiotic algae were determined for 193 coral holobionts, and the amino acid composition and δ15NAA values of selected samples were analyzed. δ15N values were influenced most by pollution stress, while C/N ratios and δ13C values depended most strongly on species. The results imply that δ13C and δ15N values are useful indicators for distinguishing the ecological niches of sympatric coral species based on microhabitat preference and resource selectivity. Using δ15NAA values, the trophic level (TL) of the examined coral samples was estimated to be 0.71 to 1.53, i.e., purely autotrophic to partially heterotrophic. Significant portions of the variation in bulk δ15N and δ13C values could be explained by the influence of heterotrophy. The TL of symbionts covaried with that of their hosts, implying that amino acids acquired through host heterotrophy are translocated to symbionts. Dependence on heterotrophy was stronger at polluted sites, indicating that the ecological role of corals changes in response to eutrophication.

Tracing the Trophic Plasticity of the Coral–Dinoflagellate Symbiosis Using Amino Acid Compound-Specific Stable Isotope Analysis

“…The trophic index, although not significantly different between autotrophic and mixotrophic coral holobionts, continuously increases from the autotrophic to the mixotrophic and heterotrophic symbionts. It thus clearly shows a strong nutritional link between the host and the symbionts, as recently acknowledged [ 22 ] and emphasizes the importance of the symbionts in the acquisition and transformation of amino acids from the external diet and the translocation to the coral host.…”

“…This positive feedback loop of symbiotic nitrogen demand would therefore turn the symbiotic compartment into a nitrogen “sink”. The assimilation of heterotrophically-acquired food by symbionts has been highlighted previously in studies, but without identifying the type of compounds acquired [ 22 , 57 , 58 ]. In [ 22 ], the authors observed that the trophic index of the symbionts of several coral species covaried with that of their host, implying that AAs acquired through host heterotrophy are translocated to the symbionts.…”

“…The secondary consumers have a TP greater than 2. In mixotrophic organisms, such as corals, which live in symbiosis with photosynthetic dinoflagellates, a TP around 1 indicates that the association is mostly autotrophic (relying on the photosynthates acquired by the dinoflagellates), while a TP higher than 1 indicates an heterotrophic input [ 22 , 38 ].…”

“…However, amino acids (AA) contain both carbon and nitrogen atoms on which CSIA can be applied. Although used only twice to study coral diet [ 21 , 22 ], CSIA-AAs have proven to be useful in paleo-studies of the tropical marine nitrogen cycle and for tracing carbon flow in reefs [ 23 , 24 ]. The δ 15 N values of consumers’ AAs give an indication of their trophic level [ 25 , 26 ] because the “source” amino acids (e.g., phenylalanine) fractionate 15 N minimally with each trophic level, while the “trophic” amino acids (e.g., glutamic acid) are markedly enriched in 15 N [ 27 , 28 ].…”

“…In corals, Fox et al [ 21 ] suggested that δ 13 C-AA ess are useful to trace coral heterotrophy, because they observed a complete separation in the δ 13 C-AA ess values between coral endosymbionts (autotrophy) and the heterotrophic nutritional sources. Fujii et al [ 22 ] used the δ 15 N AA values of several coral species sampled in natural conditions to show that their trophic levels ranged from purely autotrophic (0.71) to partially heterotrophic (1.53). Overall, these two studies show that CSIA-AAs are a promising tool for tracing coral nutritional conditions.…”