Primary producers on coral reefs : from diversity to function

Abstract

Coral reefs present a paradox: communities of rich biodiversity and abundance that flourish in environments where nutrients are scarce. Underpinning this surprising success are algae, a functional group that includes an expansive variety of forms – from single-celled phytoplankton to complex macrophytes. As dominant primary producers in marine communities, algae act as a critical nexus for ecosystem metabolism, both mediating the influx of energy and playing a principal role in nutrient retention and recycling. Primary production is constrained by nutrient availability. Under the oligotrophic conditions where corals thrive, nitrogen and phosphate limitation results in a low standing-stock of free-living algae. Algal taxa that are easily consumed are rapidly recycled through grazing and nutrient excretion, while less-digestible forms – often those that provide essential habitat-building services, such as leathery kelp and calcified crustose coralline algae – persist. The trophic powerhouse of the reef lies just underneath the surface. A mutualistic association between the endosymbiotic algae Symbiodiniaceae and their coral hosts enhances the metabolic capabilities of both partners, circumventing the restrictions otherwise imposed by nitrogen limitation: Carbon-rich photosynthates produced by Symbiodiniaceae support coral growth and calcification, while the coral provides waste ammonium, heterotrophically acquired nutrients, and an environment that enhances photosynthetic efficiency.

In this thesis, I explore the role of algae in marine biochemical cycles across multiple ecological scales – from regional variation in algal assemblages among eutrophic marine communities, to the functions provided by Symbiodiniaceae in service of nutrient acquisition and amino acid synthesis in the coral holobiont. I began by identifying how eukaryote and algal diversity are shaped by environmental gradients across a highly urbanised seascape. Through 18S rRNA metabarcoding of benthic communities sampled throughout the Pearl River Estuary, I found that water quality degradation was strongly associated with losses in red algae species, particularly among encrusting calcareous forms. The remaining research presented here utilises dual-isotope labelling of a suite of auto- and heterotrophic carbon and nitrogen sources to investigate the nutritional preferences and pathways of Acropora sp., a highly autotrophic coral. First, I traced assimilation and turnover over a three-month controlled feeding experiment through bulk stable isotope analyses (SIA) of coral and symbiont tissues. From there, I used compound-specific SIA to contrast how carbon and nitrogen from various sources are routed to amino acid synthesis and storage through coral-algal symbiosis. Collectively, these nutritional studies illustrate that host and symbiont act more independently in acquiring and utilising carbon, while nitrogen uptake and synthesis pathways involve closer coupling between partners and a greater reliance on symbiont metabolism. Only a small fraction of the autotrophic carbon shared with Acropora was assimilated into host tissue; instead, hosts preferentially utilised organic carbon derived from glucose for biosynthesis. For both partners, photosynthetic carbon was dispersed equally across all measured amino acids, while glucose-derived carbon was preferentially sunk into non-essential amino acids. In comparison, nitrogen from both inorganic (nitrate) and organic (urea) sources was heavily recycled within the holobiont, with the majority of nitrogen obtained by the holobiont being passed to symbionts for amino acid synthesis.